Ecology and Evolution

Ecological significance, biogeography and physiology of the Roseobacter group in pelagic systems

Principal investigators: Prof. Dr. Meinhard Simon, apl. Prof. Dr. Thorsten Brinkhoff

Post docs: Dr. Helge-Ansgar Giebel, Dr. Sara Billerbeck, Dr. Cristina Moraru

PhD students: Insa Bakenhus

Objective

The overall goal of this project is to elucidate the significance and function of the Roseobacter group in marine pelagic ecosystems of coastal and oceanic surface waters. During the first funding period we focus on the temperate, subpolar and polar zone and apply culture-dependent and culture-independent molecular approaches to assess the diversity and abundance, activity and functional response of relevant subclusters of this group.

The main research questions of project A1 are:

• What is the phylogenetic diversity of the Roseobacter group in pelagic ecosystems?
• What is the quantitative significance of this group and subclusters in these ecosystems and relative to other bacterioplankton groups?
• Are the Roseobacter subclusters and populations metabolically more active than other bacterioplankton groups and if so, under which environmental conditions?
• What are specific biogeochemical and metabolic functions of subclusters of this group in these ecosystems?
• What is the quantitative significance of Roseobacter-specific biogeochemical functions in pelagic ecosystems? (CO oxidase, AAP)
• Do specific interactions of distinct Roseobacter populations with distinct algal populations exist and if so, what kind of interactions?

Projects

• Biogeography of pelagic Roseobacter subcluster (S. Billerbeck, I. Bakenhus)
• Isolation and characterisation of pelagic Roseobacter strains (H.-A. Giebel / S. Billerbeck)
• Genome sequencing of pelagic roseobacters (H.-A. Giebel, S. Billerbeck, I. Bakenhus; in cooperation with project A3/Z02)
• Aerobic, anoxygenic photosynthesis in Planktomarina temperata (H.-A. Giebel)

Methods

• Sampling the water column and mesocosm experiments onboard different reserch vessels
• PCR with primers specific for the Roseobacter group and relevant subclusters to analyse their distribution in global oceans
• Cluster Analysis of DGGE gels to determine the diversity of the Roseobacter group
• 454 – Pyrosequencing / Illumina sequencing to get an insight in the diversity and abundance of Roseobacter subclusters (in cooperation with A3/Z02)
• (CARD-, MAR-, BrdU-) FISH for quantitative analyses on group or species level of bacteria or roseobacters and to link that to substrate specific activities
• Flow Cytometry is used for cell counting of bacterial and algal cells of in situ or culture samples and for analyses of their population dynamics
• Isolation of new pelagic roseobacters via dilution cultures with different minimal media
• Genome analysis of newly isolated roseobacters

Hydrographic and Biogeochemical parameters analysed during the cruises

• CTD (salinity, temperature, depth, fluorescence, turbidity)
• Chla, phaeopigments
• DOC, TDN, DOM
• Nutrients (NO_x,NO₂, PO₄, SiO₄)
• POC, PON
• Amino acids (DAA, TAA)
• Carbohydrates (DFCHO, TCHO)
• Phytoplankton quantitative
• Phytoplankton autofluorescence
• Bacterial cell numbers (live measurement onboard by flow cytometry)
• Bacterial DNA, RNA
• (CARD-/MAR-/BrdU-) FISH
• Grazing of specific bacterial groups
• Bacterial production, substrate turnover rates

Expeditions:

DateExpedition

26.01.-27.02.2017

RV Sonne (SO254), Southwest Pacific, Auckland (New Zealand) - Auckland (more information)

01.05.-03.06.2016

RV Sonne (SO248), Pacific transect, Auckland (New Zealand) - Dutch Harbour (Alaska)

23.05.-06-06.2014

RV Heincke (HE425), North Sea transect

10.4.-15.5.2012

RV Polarstern (ANT-XVIII/5), Atlantic transect, Punta Arenas (Chile) - Bremerhaven (Cruise report)

14.3.-9.4. 2012

RV Polarstern (ANT-XXVIII/4), Southern Ocean, Punta Arenas (Chile) - Antarctic Penninsula and back (Cruise report)

3.12.2011-5.1.2012

RV Polarstern (ANT-XXVIII/2), Southern Ocean, Kapstadt (South Afrika) - Neumeyer-Station and back (Cruise report)

12.-29.7. 2011

RV Heincke (HE361), North Sea transect

25.-31. 5. 2010

RV Heincke (HE327), German Bight

International Cooperations

• Prof. Jang-Cheon Cho, Inha University, Incheon, Korea
• Prof. Dr. Feng Chen, University of Maryland, Baltimore USA
• Dr. Sijun Huang, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China
• Prof. Lone Gram, National Food Institute, Technical University of Denmark, Lyngby, Denmark
• Prof. Wade Jeffrey, Center for Environmental Diagnostics and Bioremediation, University of West Florida, Pensacola, United States of America

Bachelor, Master and PhD theses

• Klotz, Franziska (Master, 2016). Characterization of "Tritonibacter horizontis", isolated from seawater after the Deepwater Horizon oil spill.

• Billerbeck, Sara (PhD, 2016). The pelagic clusters of the Roseobacter group: Global distribution, genome analysis and physiological characterization.

• Dlugosch, Leon (Master, 2016). Bacterioplankton community composition and growth activity during early summer in the North Sea.

• Orchard, Julia (Master, 2014). Physiological Characterization of "Candidatus Octadecabacter temperatus" SB1.

• Jongmans, Elanor (Master, 2014). Phylogeny-based evaluation of pufM gene specific primer systems.

• Milke, Felix (Bachelor, 2014). Hydrographic, chemical and microbial characterization of the pelagic North Sea in early summer.

• Tran, Quoc Den (Master, 2014). Quantification of DNA-synthesizing cells in bacterial communities of the North Sea by BrdU-FISH.

• Hahnke, Sarah (PhD, 2012). Physiological characterization and molecular ecological investigation of diverse organisms of the Roseobacter clade isolated from the North Sea.

• Kalhöfer, Daniela (PhD, 2012). Genome analysis and comparative genomics of host-associated bacteria of the marine Roseobacter clade.

• Aydogmus, Ozan (Master, 2011). Development of specific molecular biological detection systems for a distinct population of a pelagic Roseobacter isolate (SH36).

• Bakenhus, Insa (Bachelor, 2011). Quantifizierung von aktiven Roseobacter spp. in der Nordsee mittels Bromodesoxyuridin Inkorporation und Fluoreszenz in situ Hybridisierung (BrdU-FISH).

• Wienhausen, Gerrit (Bachelor, 2011). Vorkommen von Untergruppen der Roseobacter-Gruppe in der Deutschen Bucht.

• Pockels, Lina (Bachelor, 2010). Biogeografische Verteilung der Gattung Roseobacter und Taurinverwertung durch Roseobacter litoralis.

Publications

2017

• Bakenhus I, Voget S, Poehlein A, Brinkhoff T, Daniel R, Simon M (2017). Genome sequence of Planktotalea frisia type strain (SH6-1^T), a representative of the Roseobacter group isolated from the North Sea during a phytoplankton bloom. Stand Gen Sci (submitted).

• Milici M, Vital M, Tomasch J, Badewien TH, Giebel H-A, Plumeier I, Wang H, Pieper DH, Wagner-Döbler I, Simon M. (2017) Diversity and community composition of particle-associated and free-living bacteria in mesopelagic and bathypelagic Southern Ocean water masses: evidence of dispersal limitation in the Bransfield strait. Limnol Oceanogr 62: 1080-1095.

• Simon M, Scheuner C, Meier-Kolthoff JP, Brinkhoff T, Wagner-Döbler I, Ulbrich M, Klenk HP, Schomburg D, Petersen J, Göker M. (2017) Phylogenomics of Rhodobacteraceae reveals evolutionary adaptation to marine and non-marine habitats. ISME 11: 1483-1499.

2016

• Billerbeck S, Wemheuer B, Voget S, Poehlein A, Giebel H-A, Brinkhoff T, Gram L, Jeffrey W H, Daniel R, Simon M (2016). Biogeography and environmental genomics of the Roseobacter-affiliated pelagic CHAB-I-5 lineage. Nat. Microbiol. Article 16063.

• Giebel HA, Klotz F, Voget S, Poehlein A, Grosser K, Teske A, Brinkhoff T (2016) Draft genome sequence of the marine Rhodobacteraceae strain O3.65, cultivated from oil-polluted seawater of the Deepwater Horizon oil spill. Stand Genomic Sci 11:81-93.

• Kanukollu S, Wemheuer B, Herber J, Billerbeck S, Lucas J, Daniel R, Simon M, Cypionka H, Engelen B (2016) Distinct compositions of free-living, particle-associated and benthic communities of the Roseobacter group in the North Sea. FEMS Microbiol Ecol. 92/1: Article fiv145.

• Klingner A, Bartsch A, Dogs M, Wagner-Döbler I, Jahn D, Simon M, Brinkhoff T, Becker J, Wittmann C (2015) Large-scale ¹³C flux profiling reveals conservation of the Entner-Doudoroff pathway as a glycolytic strategy among marine bacteria that use glucose. Appl Environ Microbiol 81/7: 2408-2422.

• Milici M, Deng1 ZL, Tomasch J, Decelle J, Wos-Oxley M, Wang H, Jáuregui R, Plumeier I, Giebel H-A, Badewien H, Wurst M, Pieper P, Simon M, Wagner-Doebler I (2016) Co-occurrence analysis of microbial taxa in the Atlantic Ocean reveals high connectivity in the free-living bacterioplankton. Frontiers Microbiol. 7: Article 649.

• Milici M, Tomasch J, Wos-Oxley M, Decelle J, Jáuregui R, Wang H, Deng ZL, Plumeier I, Giebel H-A, Badewien T, Wurst M, Pieper DH, Simon M, Wagner-Doebler I (2016) Bacterioplankton biogeography in the Atlantic Ocean: a case study of the distance-decay relationship. Frontiers Microbiol. 7: Article 590.

• Milici M, Tomasch J, Wos-Oxley ML, Wang H, Jáuregui R, Camarinha-Silva A, Deng ZL, Plumeier I, Giebel H-A, Wurst M, Pieper DH, Simon M, Wagner-Döbler I (2016) Low diversity of planktonic bacteria in the tropical ocean. Scientific Reports 6: Article 19054.

• Mitulla M, Dinasquet J, Guillemette R, Simon M, Azam F, Wietz M (2016) Response of bacterial communities from California coastal waters to alginate particles and an alginolytic Alteromonas macleodii strain. Environ Microbiol, online first (doi:10.1111/1462-2920.13314).

• Osterholz H, Singer G, Wemheuer B, Daniel R, Simon M, Niggemann J, Dittmar T (2016) Deciphering associations between dissolved organic molecules and bacterial communities in a pelagic marine system. ISME J 7: 1717-1730.

• Zhan Y, Huang S, Voget S, Simon M, Chen F (2016) A novel Roseobacter phage possesses features of podoviruses, siphoviruses, prophages and gene transfer agents. Scientific Reports 6: 30372 (DOI: 10.1038/srep30372). 

2015

• Billerbeck S, Orchard J, Tindall B J, Giebel H-A, Brinkhoff T, Simon M (2015). Description of Octadecabacter temperatus sp . nov ., isolated from the southern North Sea , emended description of the genus Octadecabacter and reclassification of Octadecabacter jejudonensis Park & Yoon 2014 as Pseudooctadecabacter jejudonensis. Int. J. Syst. Evol. Microbiol. 1967–1974.

• Voget S, Wemheuer B, Brinkhoff T, Vollmers J, Dietrich S, Giebel H-A, Beardsley C, Sardemann C, Bakenhus I, Billerbeck S, Daniel R, Simon M (2015). Adaptation of an abundant Roseobacter RCA organism to pelagic systems revealed by genomic and transcriptomic analyses. ISME J. 9: 371-384.

• Voget S, Billerbeck S, Simon M, Daniel R (2015). Closed genome sequence of Octadecabacter temperatus SB1, the first mesophilic species of the genus Octadecabacter. Genome Announc 3(5): e01051-15. (doi:10.1128/genomeA.01051-15).

• Klingner A, Bartsch A, Dogs M, Wagner-Döbler I, Jahn D, Simon M, Brinkhoff T, Becker J, Wittmann C (2015) Large-scale ¹³C flux profiling reveals conservation of the Entner-Doudoroff pathway as a glycolytic strategy among marine bacteria that use glucose. Appl Environ Microbiol 81/7: 2408-2422.

• Neumann AM, Balmonte JP, Berger M, Giebel H-A, Arnosti C, Voget S, Simon M, Brinkhoff T, Wietz M (2015) Different utilization of alginate and other algal polysaccharides by marine Alteromonas macleodii ecotypes. Environ Microbiol 17/10: 3857-3868.

• Osterholz H, Niggemann J, Giebel H-A, Simon M, Dittmar T (2015) Inefficient microbial production of refractory dissolved organic matter in the ocean. Nature Comm 6: 7422.

• Schwedt A, Seidel M, Dittmar T, Simon M, Bondarev V, Romano S, Lavik G, Schulz-Vogt HN (2015) Substrate use of Pseudovibrio sp. growing in ultraoligotrophic seawater, PLOS One, 10(3): e0121675 (doi:10.1371/journal.pone.0121675).

• Wietz M, Wemheuer B, Simon H, Giebel H-A, Seibt MA, Daniel R, Brinkhoff T, Simon M (2015) Polysaccharides initiate distinct responses of bacterial communities from the Southern and Atlantic Oceans. Environ Microbiol 17/10: 3822-3831.

2014

• Wemheuer B, Güllert S, Billerbeck S, Giebel H-A, Voget S, Simon M, Daniel R (2014) Impact of a phytoplankton bloom on the diversity of the active bacterial community in the southern North Sea as revealed by metatranscriptomic approaches. FEMS Microbiol Ecol 87: 378-389 (DOI: 10.1111/1574-6941.12230).

2013

• Hahnke S, Brock NL, Zell C, Simon M, Dickschat JS, Brinkhoff T (2013a). Physiological diversity of Roseobacter clade bacteria co-occurring during a phytoplankton bloom in the North Sea. System. Appl. Microbiol. 36: 39– 48.
• Hahnke S, Sperling M, Langer T, Wichels A, Gerdts G, Beardsley C, Brinkhoff T, Simon M (2013b) Distinct seasonal growth patterns of the bacterium Planktotalea frisia in the North Sea and specific interactions with phytoplankton algae. FEMS Microbiol Ecol, 86: 185-199.

• Giebel H-A, Kalhoefer D, Gahl-Janssen R, Choo YJ, Lee K, Cho JC, Tindall BJ, Rhiel E, Beardsley C, Aydogmus Ö O, Voget S, Daniel R, Simon M, Brinkhoff T (2013). Planktomarina temperata gen. nov., sp. nov., belonging to the globally distributed RCA cluster of the marine Roseobacter clade, isolated from the German Wadden Sea. Inter. J. System. Evol. Microbiol. 63: 4207–4217.
• Vollmers J, Voget S, Dietrich S, Gollnow K, Smits M, Meyer K, Brinkhoff T, Simon M, Daniel R (2013) Poles apart: Extreme genome plasticity and a new xanthorhodopsin-like gene family in the genomes of Octadecabacter arcticus 238 and Octadecabacter antarcticus 307. PLoS One 8(5): e63422PLoS One.

2012

• Simon M, Billerbeck S, Kessler D, Selje N, Schlingloff A (2012). Bacterioplankton communities in the Southern Ocean: Composition and growth response to various substrate regimes. Aquat. Microb. Ecol. 68:13–28.

2011

• Kalhoefer D, Thole S, Voget S, Lehmann R, Liesegang H, Wollher A, Daniel R, Simon M, Brinkhoff T (2011). Comparative genome analysis and enhanced physiological description of Roseobacter litoralis. BMC Genomics 12: 324.

Other Publications

• Beardsley C, 12 co-authors, Simon M (2012) The Roseobacter clade and the dissolved organic matter (DOM) composition in the Atlantic sector of the Southern Ocean. In: Kattner G (ed) The expedition of the Research Vessel "Polarstern" to the Antarctic in 2012 (ANT-XXVIII/2) Reports on Polar and Marine Research 646: 36-39.
• Simon M, and 13 co-authors (2012) In: Bumke K (ed) The expedition of the Research Vessel "Polarstern" to the Antarctic in 2012 (ANT-XXVIII/5) Reports on Polar and Marine Research 654: 30-35.
• Simon, M, and 11 co-authors (2012) Composition and activity of the bacterioplankton communities in the Drake Passage and Antarctic Peninsula region with a special emphasis on the Roseobacter clade and dissolved organic matter. In: Lucassen M (ed) The expedition of the Research Vessel "Polarstern" to the Antarctic in 2012 (ANT-XXVIII/4) Reports on Polar and Marine Research 653: 49-54.

Presentations at national and international symposia

• Bakenhus, I., Wietz, M., Giebel, H.-A., Beardsley, C., Simon, M. 2016. Bacterioplankton biogeography and activity patterns in the Southern Ocean. Symposium of the International Society for Microbial Ecology (ISME) Montreal, Canada, 22-26.August (talk).

• Billerbeck S., Voget S., Wemheuer B., Poehlein A., Giebel H.-A., Brinkhoff T., Daniel R., Simon M. 2016. Biogeography and environmental genomics of the Roseobacter group affiliated CHAB-I-5 lineage. Symposium of the International Society for Microbial Ecology (ISME), Montreal, Canada, 22-26.August (poster).

• Bakenhus, I., Giebel, H.-A., Wemheuer, B., Wietz, M., Dlugosch, L., Simon, M. 2015. Bacterioplankton community composition and activity patterns across a latitudinal transect from Antarctica (70°S) to the North Atlantic (47°N). Symposium on Aquatic Microbial Ecology (SAME), Uppsala (talk).

• Giebel, H.-A., Schlingloff, A., Simon, M., Brinkhoff, T. 2015. Physiological vs. genomic features of the Roseobacter clade affiliated (RCA) cluster: What we can learn from cultivation-approaches with Planktomarina temperata. Symposium on Aquatic Microbial Ecology (SAME), Uppsala (poster).

• Bakenhus, I., Giebel, H.-A., Wurst, M., Beardsley, C., Simon, M., Wietz, M. 2015. Bacterioplankton biogeography and activity in the Southern Ocean. Annual Meeting of the German Society of General and Applied Microbiology (VAAM), Marburg (poster).

• Giebel, H.-A., B. Wemheuer, S. Voget, R. Daniel and M. Simon. 2014. The abundant Roseobacter clade affiliated (RCA) cluster: Metabolic traits of its model organism Planktomarina temperata RCA23. 17th Ocean Sciences Meeting (OSM, co-sponsored by the American Society of Limnology and Oceanography (ASLO)), Honolulu, Hawaii, USA, February 23-28. (book of abstracts, p. 118, poster).

• Simon, M., B. Wemheuer, H.-A. Giebel, S. Billerbeck, M. Wurst, R. Daniel. 2014. Highly productive and active bacterioplankton communities in the southern ocean in austral fall. 17th Ocean Sciences Meeting (OSM, co-sponsored by the American Society of Limnology and Oceanography (ASLO)), Honolulu, Hawaii, USA, February 23-28. (book of abstracts, p. 79, talk).

• Busch, M., F. Peiffer, Giebel, H.-A., H. Hillebrand, S. Moorthi. 2014. Effects of nutrient concentrations, phagotrophic feeding and alleopathy on bloom dynamics of potentially harmful dinoflagelates. 17th Ocean Sciences Meeting (OSM, co-sponsored by the American Society of Limnology and Oceanography (ASLO)), Honolulu, Hawaii, USA, February 23-28. (book of abstracts, p. 140, talk).

• Giebel, H.-A., B. Wemheuer, S. Voget and M. Simon. 2013. Benefits of aerobic anoxygenic photosynthesis for the Roseobacter clade affiliated (RCA) cluster. 1st EMBO conference on Aquatic Microbial Ecology (SAME13), Stresa, Italy, 8-13 September 2013. (book of abstracts, p. 219, poster).

• Simon, M. et al. (2013). Progress report and future perspectives of project A1. 7^th status semimar of TRR 51, HWK Delmenhorst, Germany, 15-66 October 2013. (talk).

• Billerbeck, S., B. Wemheuer, H.-A. Giebel, R. Daniel and M. Simon. 2013. Distribution and abundance of clusters of the Roseobacter clade in the North Sea. 1^st EMBO conference on Aquatic Microbial Ecology (SAME13), Stresa, Italy, 8-13 September 2013. (book of abstracts, p. 225, poster).

• M. Simon, B. Wemheuer, H.-A. Giebel, T. Brinkhoff, C. Beardsley, I. Bakenhus, R. Daniel and S. Voget. 2013. Major role of photoheterotrophic and CO oxidizing Roseobacter RCA population in the ocean. 1^st EMBO conference on Aquatic Microbial Ecology (SAME13), Stresa, Italy, 8-13 September 2013. (book of abstracts, p. 69, talk).

• Giebel, H-A. et al. (2013). Benefits of aerobic anoxygenic photosynthesis for growth of Cand. Planktomarina temperata of the Roseobacter clade affiliated (RCA) cluster. International Symposium: Research highlights and reports of the first funding period of TRR 51, HWK Delmenhorst, Germany, 24-26 June 2013, (talk).

• Simon, M. et al. (2013). Progress report. International Symposium: Research highlights and reports of the first funding period of TRR 51, HWK Delmenhorst, Germany, 24-26 June 2013, (talk).

• Giebel, H.-A., B. Wemheuer, S. Voget, and M. Simon. 2013. Turn on the lights: Benefits of aerobic anoxygenic photosynthesis for the Roseobacter clade affiliated (RCA) cluster. Annual Meeting of the German Society of General and Applied Microbiology (VAAM) together with KNVM, Bremen, Germany, May 10-13. (book of abstracts, p. 176, poster).

• Simon, M. , T. Brinkhoff, B. Wemheuer, H.-A. Giebel, C. Beardsley, I. Bakenhus, R. Daniel and S. Voget. 2013. Major role of photoheterotrophic and CO oxidizing Roseobacter RCA population in the ocean. Annual Meeting of the German Society of General and Applied Microbiology (VAAM) together with KNVM, Bremen, Germany, May 10-13. (book of abstracts, p. 163, talk).

• Billerbeck, S., H.-A. Giebel, T. Brinkhoff, C. Beardsley, L. Gram, W.H. Jeffrey and M. Simon. 2013. Distribution of clusters of the Roseobacter clade in global oceans. Annual Meeting of the German Society of General and Applied Microbiology (VAAM) together with KNVM, Bremen, Germany, May 10-13. (book of abstracts, p. 164, talk).

• Simon, M. (2012). A1 Progress report and future perspectives. 7^th Status Seminar of the Transregio 51, Oktober 15-16, HWK Delmenhorst, Germany (talk).

• Simon, M. 2012. The Roseobacter clade and its potential significance for the microbial carbon pump. Workshop SCOR WG 134: The Microbial Carbon Pump in the Ocean, Delmenhorst, Germany, August 26-28.

• Giebel, H.-A., B. Wemheuer, S. Voget, and M. Simon. 2012. The Roseobacter clade affiliated (RCA) cluster: Do these microbes conduct aerobic anoxygenic photosynthesis? 14^th Symposium of the International Society for Microbial Ecology (ISME), The power of the small, Copenhagen, Denmark, August 19-24. (book of abstracts, poster).

• Simon, M., T. Brinkhoff, B. Wemheuer, H.-A. Giebel, C. Beardsley, I. Bakenhus, R. Daniel and S. Voget. 2012. Evidence for ocean-wide distribution of an abundant photoheterotrophic and CO oxidizing RCA roseobacter population in the North Sea and North Atlantic. 14^th Symposium of the International Society for Microbial Ecology (ISME), The power of the small, Copenhagen, Denmark, August 19-24. (book of abstract, talk).

• Simon, M., B. Wemheuer, H.-A. Giebel, T. Brinkhoff, C. Beardsley, R. Daniel and S. Voget. 2012. Genomic features and distribution of an abundant photoheterotrophic and CO oxidizing RCA isolate in the North Sea and North Atlantic. Gordon Research Conferences (GRC), Marine Microbes - Bridging the Gaps from Genomes to Biomes, Lucca (Barga), Italy, June 24-29. (book of abstract, poster).

• Billerbeck, S., H.-A. Giebel and M. Simon. 2012. Occurence of Roseobacter subclusters in the North Sea. Gordon Research Conferences (GRC), Marine Microbes - Bridging the Gaps from Genomes to Biomes, Lucca (Barga), Italy, June 24-29. (book of abstract, poster).

• Giebel, H-A. (2012). Science and life on board the RV Polarstern during cruises ANT-XXVIII/4&5. 6^th Status Seminar of the Transregio 51, 5^th June 2012, HZI Braunschweig, Germany (talk).

• Simon, M. (2012). Polarstern cruise from Punta Arenas to the Southern Ocean and across the Atlantic back to Bremerhaven, 14 Mar – 15 May 2012 – report and first results. 6^th Status Seminar of the Transregio 51, 5^th June 2012, HZI Braunschweig, Germany (talk).

• Giebel, H-A. and J. Vollmers (2012). Sampling of roseobacters in the Southern Ocean - cience and life on board the RV Polarstern cruise ANT-XXVIII/2 -report and first results. 5^th Status Seminar of the Transregio 51, 6^th June 2012, HZI Braunschweig, Germany (talk).

• Giebel, H.-A., B. Wemheuer, S. Voget, and M. Simon. 2011. First hints for conducting aerobic anoxygenic photosynthesis by bacteria of the Roseobacter clade affiliated (RCA) cluster. 12^th Symposium on Aquatic Microbial Ecology (SAME), Rostock-Warnemünde, Germany, August 28-September 2. (book of abstracts, p. 225, poster).

• Billerbeck, S., H.-A. Giebel, and M. Simon. 2011. Occurrence of Roseobacter subclusters in the German Bight of the North Sea. 12^th Symposium on Aquatic Microbial Ecology (SAME), Rostock-Warnemünde, Germany, August 28-September 2. (book of abstracts, p. 138, poster).

• Simon, M., S. Hahnke, H.-A. Giebel, S. Simon, H. Osterholz, and T. Brinkhoff. 2011. Physiology and interactions of phytoplankton-assosiated roseobacters. 12^th Symposium on Aquatic Microbial Ecology (SAME), Rostock-Warnemünde, Germany, August 28-September 2. (book of abstracts, p. 113, talk).

• Beardsley, C. 2011. International workshop: Fluorescence in situ hybridisation (1^st FISH camp), MPI, Bremen, Germany, June 14-24.

• Billerbeck, S., H.-A. Giebel and M. Simon. 2011. Occurrence of Roseobacter subclusters in the German Bight of the North Sea. Annual Meeting of the German Society of General and Applied Microbiology (VAAM), Karlsruhe, Germany, April 3-6. (book of abstracts, p. 110, poster).

• Langer, T., S. Hahnke, T. Brinkhoff and M. Simon. 2011. Response of the Roseobacter clade to an experimentally-induced Phaeocystis bloom. Annual Meeting of the German Society of General and Applied Microbiology (VAAM), Karlsruhe, Germany, April 3-6. (book of abstracts, p. 171, poster).

• Simon, M. 2011. Decomposition of humic acids by estuarine and marine bacterial communities. Ocean Science Meeting (co-sponsored by the American Society of Limnology and Oceanography (ASLO)), San Juan, Puerto Rico, February 19-20.

• Billerbeck, S. (2010). Ecological significance, biogeography and physiology of the Roseobacter group in pelagic systems. 1^st Status Seminar of the Transregio 51, 21^st October 2010, HZI Braunschweig, Germany (talk).

• Simon, M., Giebel, H.-A., Voget, S., Kalhoefer, D., Daniel, R. and T. Brinkhoff. 2010. The Roseobacter RCA cluster in the North Sea - population dynamics, physiological and genomic properties. 13^th Symposium of the International Society for Microbial Ecology (ISME), Stewards of a changing planet, Seattle, WA, USA, August 22-27. (book of abstracts, poster).

• Giebel, H.-A., D. Kalhoefer, S. Voget, T. Brinkhoff and M. Simon. 2010. Distribution of Roseobacter RCA and SAR11 lineages in the Southern Ocean and North Sea and characteristics of an abundant RCA isolate. Gordon Research Conferences (GRC), Marine Microbes: From Genes To Global Cycles, Tilton, NH, USA, July 4-9. (book of abstracts, poster).

• Giebel, H.-A., D. Kalhoefer, H. Osterholz, S. Voget, T. Brinkhoff and M. Simon. 2010. The Roseobacter clade affiliated (RCA) cluster: Its occurence, diversity and potential significance in marine habitats. Transregional Collaborative Research Center (TRR-51) Kick-off Symposium: Ecology, Physiology and Molecular Biology of the Roseobacter clade: Towards a Systems Biology Understanding of a Globally Important Clade of Marine Bacteria, Delmenhorst, Germany, June 13-15. (book of abstracts, talk).

• Hahnke, S., H.-A. Giebel, M. Sperling, H. Osterholz, M. Simon and T. Brinkhoff. 2010. Physiology and biogeography of phytoplankton-associated roseobacters. Transregional Collaborative Research Center (TRR-51) Kick-off Symposium: Ecology, Physiology and Molecular Biology of the Roseobacter clade: Towards a Systems Biology Understanding of a Globally Important Clade of Marine Bacteria, Delmenhorst, Germany, June 13-15. (book of abstracts, talk).

• Giebel, H.-A., D. Kalhoefer, H. Osterholz, S. Voget, T. Brinkhoff and M. Simon. 2010. The Roseobacter clade affiliated (RCA) cluster: Its occurence, diversity and potential significance. International workshop: The microbial view of marine biogeochemical cycles, Banyuls-sur-Mer, France, May 19-21. (book of abstracts, talk).

• Simon, M., S. Hahnke, H.-A. Giebel, H. Osterholz and T. Brinkhoff. 2010. Drivers of organic matter turnover in the sea - some examples from the Roseobacter clade. International workshop: The microbial view of marine biogeochemical cycles, Banyuls-sur-Mer, France, May 19-21. (book of abstracts, talk).

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Distribution, metabolic capacities and phage-host interactions of the Roseobacter group in marine sediments

Principal investigators: Dr. Bert Engelen 

PhD student: Dennis Tebbe, Marion Pohlner

Former PhD students: Judith Lucas, Saranya Kanukollu

Former master students: Julius Degenhardt, Janina Herber, Nawras Ghanem

Objective: 

Roseobacter-affiliated bacteria represent a numerically significant part not only of pelagic, but also of benthic microbial communities. Thus, we want to understand their biogeography, distribution, abundance and main activities in marine sediments. So far, we have analyzed samples from the North Sea (Heincke cruise HE361), the Antarctic Peninsula (Polarstern cruise ANT28/4) and the Pacific Ocean (Sonne cruises SO248 and SO254) to identify regional differences and a putative overlap between free water, particles and the sediment surface. In order to identify the metabolic activity of roseobacters, ribosomal RNA based analyses are performed by Digoxygenin-labeled UTP incorporation. Here, we will identify the factors that affect their occurrence and their metabolic response to changes at the oxic/anoxic transition zone. These experiments are currently running with special emphasis on their sulfur metabolism.

Methods:

Cultivation

• Original samples obtained directly from various sites are transferred in media amended with DMS, DMSP and DMSO. All cultivations are  performed in serial dilutions (MPN)

Diversity and distribution of the Roseobacter group

• Total cell counts (original and MPN enrichments) with SYBR Green I quantification.
• CARD-FISH by using both, EUB388 and ROS536R probes
• qPCR by using Bacteria and Roseobacter-specific primers
• Cluster analysis of DGGE gels
• 454- and Illumina-Sequencing

Metabolic activity tests

• Quantitative (real-time) PCR
• In vivo labeling of bacterial rRNA by incorporating DIG-11-UTP and separation by magnetic beads
• Parallel verification of the results by stable isotope probing (SIP)

Expeditions:

• Expedition SO254 (RV Sonne, February 2017): Functional diversity of bacterial communities and the metabolome in the water column, sediment and in sponges in the southwest Pacific around New Zealand - Microbial abundance, diversity and activity in Pacific Deep Sea sediments
• Expedition SO248 (RV Sonne, May 2016): Ductional diversity of bacterial communities and the geometabolome in the central and north Pacific - Microbial abundance, diversity and activity in Pacific Deep Sea sediments
• Expedition ANT28/4 (RV Polarstern, March-April 2012): The Roseobacter clade and the DOM composition in the Drake Passage and the Antarctic Peninsula region of the Southern Ocean
• Expedition HE361 (RV Heincke, June 2011): Sampling two transects along the German/Danish coast and the Norwegian channel

Contributions at (inter)national conferences:

• VAAM conference (15–18 April 2018, Wolfsburg): The distribution of benthic Roseobacter group members in the Pacific is shaped by nutrient availability at the seafloor and productivity in the water column (Poster)
• ISME conference (21-26 August 2016, Montreal): The Roseobacter group in marine sediments - abundance, diversity and metabolic potential (Poster)
• VAAM conference (13–16 March 2016, Jena): Defining unknown members of the Roseobacter group in marine sediments (Poster)
• VAAM conference (01-04 March 2015, Marburg): Distinctive distribution of free-living, particle-associated and benthic Roseobacter populations (Talk) and Identification of metabolically active microbial communities in sediments by two independent RNA-based in vivo labeling techniques (Poster) 
• ISME conference (24-29 August 2014, Seoul): Specific distribution of Roseobacter populations from the water column down to the sediments of a coastal sea (Poster)
• VAAM conference (10-13 March 2013, Bremen): Spatial distribution and diversity of the Roseobacter clade in temperate and permanently cold marine sediments (Poster)

International collaboration:

• Brandi Kiel-Reese, Texas A&M University - Corpus Christi, Texas, USA
• Heath Mills, University of Houston - Clear Lake, Texas, USA
• Hendrik Schäfer, University of Warwick, United Kingdom

Master thesis:

• Degenhardt, Julius (March 2017): Abundance and diversity of the Roseobacter group within deap-sea sediments along a transect from Nez Zealand to Alaska
• Ghanem, Nawras (April 2013): Adundance and distribution of Roseobacter-affiliated bacteria in Antarctic sediments
• Herber, Janina (November 2012): Abundance and diversity of Roseobacter-affiliated bacteria in sediment and water samples of the North Sea

PhD thesis:

• Kanukollu, Saranya (2016): The metabolic potential and the distribution of the Roseobacter group in marine sediments

Publications:

• Kanukollu S, Ghanem N, Wemheuer B, Erlmann N, Schnetger B, Köster J, Pohlner M, Daniel R, Cypionka H, Engelen B The seafloor around the South Shetland Islands exhibits a shift in diversity of benthic bacteria and the Roseobacter group with increasing water and sediment depth (submitted to Polar Research)
• Pohlner M, Degenhardt J, von Hoyningen-Huene A, Wemheuer B, Erlmann N, Schnetger B, Engelen B (2017) The biogeographical distribution of benthic Roseobacter group members along a Pacific transect is linked to oceanic provinces with comparable nutrient composition. Front Microbiol 8: 2550, https://doi.org/10.3389/fmicb.2017.02550.
• Pohlner M, Marshall I, Schreiber L, Cypionka H, Engelen B (2017) Draft genome sequence of Pseudoruegeria sp. SK021, a representative of the marine Roseobacter group, isolated from North Sea sediment. Genome A 5:e00541-17, https://doi.org/10.1128/genomeA.00541-17.
• Harig T, Schlawis C, Ziesche L, Pohlner M, Engelen B, Schulz S (2017) Nitrogen-containing volatiles from marine Salinispora pacifica and Roseobacter-group bacteria. J Nat Prod, https://doi.org/10.1021/acs.jnatprod.7b00789.
• Kanukollu S, Voget S, Pohlner M, Vandieken V, Petersen J, Kyrpides NC, Woyke T, Shapiro N, Göker M, Klenk H-P, Cypionka H, Engelen B (2016) Genome sequence of Shimia sp. SK013, a representative of the Roseobacter group isolated from marine sediment. SIGS 11:1-10, https://doi.org/10.1186/s40793-016-0143-0.
• Kanukollu S, Wemheuer B, Herber J, Billerbeck S, Lucas J, Daniel R, Simon M, Cypionka H, Engelen B (2016) Distinct compositions of free-living, particle-associated and benthic communities of the Roseobacter group in the North Sea. FEMS Microbiol Ecol. 92/1: fiv145, https://doi.org/10.1093/femsec/fiv145.
• Soora M, Tomasch J, Wang H, Michael V, Petersen J, Engelen B, Wagner-Döbler I, Cypionka H (2015) Oxidative stress and starvation in Dinoroseobacter shibae: The role of extrachromosomal elements. Front Microbiol 6: 233, https://doi.org/10.3389/fmicb.2015.00233.
• Sass H, Köpke B, Rütters H, Feuerlein T, Dröge S, Cypionka H, Engelen B (2010) Tateyamaria pelophila sp. nov. a facultatively anaerobic Alphaproteobacterium isolated from tidal-flat sediments, and emended descriptions of the genus Tateyamaria and of Tateyamaria omphalii. Int J Sys Evol Microbiol 60: 1770-1777, https://doi.org/10.1099/ijs.0.013524-0.

Z02: Assessment and exploitation of the metabolic potentials and the molecular characterization of uncultivated members of the Roseobacter clade

Principal Investigators: Prof. Dr. Rolf Daniel

Post-Doc: Birgit Pfeiffer

PhD student: Florian Lenk

Associated scientists: Dr. Anja Poehlein, Dr. Bernd Wemheuer

Objective

In this subproject, the genomic potential and important functions of Roseobacter populations will be analyzed by culture-independent metagenomic and metatranscriptomic approaches. To identify indigenous gene- and taxon-specific patterns and key metabolic functions comparative metabolic and functional profiling of representative samples from the North Sea, the Southern Ocean, biofilms, and mesocosms will be performed by employing large-scale pyrosequencing. The mesocosm experiments will be focused on the effect of addition of organic sulfur compounds, defined phytoplankton algae, or organic compounds on the functional and phylogenetic structure of the community. The influence of incubation at light and dark as well as different salinities and pH values will be also evaluated. For metagenomic sequence analysis and for metatranscriptomic analyses, DNA and RNA, respectively, will be isolated from all samples, simultaneously. In addition, metagenomic libraries are constructed and screened for important functions such as genes involved in quorum sensing, energy metabolism, production of secondary metabolites and the corresponding regulatory networks. The large-insert libraries are also screened for phylogenetic anchors such as 16S rRNA genes. Recombinant fosmids harbouring 16S rRNA genes are sequenced. In this way, a phylogenetic marker is linked to other genes of the same organisms. This approach will be extended to other marker genes and gene clusters. These studies in close cooperation with the results of the systems biology approaches to model organism allow a partial genome characterization of uncultivated roseobacters via comparison to the data obtained for the cultivated Roseobacter strains. The distribution and variability of certain genes and pathways in environmentally abundant members of the Roseobacter group are mirrored. In this way, generated systems biology models from other subprojects can be extended to uncultivated Roseobacter clade bacteria.

Role in the CRC/General Methods

Together with A5, A6, and A7, we concentrate on different aspects of genomic research (Fig. 1). In A3, we focus on metagenomics.

Fig. 1: Our role in the CRC.

We apply different metagenomic and metatranscriptomic approaches to study the Roseobacter clade in situ (Fig. 2). In addition, we also analyse the genome of certain Roseobacter isolates (with focus on the genus Octadecabacter and differernt members of so far underreprestend subclusters).

Fig. 2: Applied Methods. (For further reading: Simon C, Daniel R (2011) Metagenomic analyses: past and future trends. Appl Environ Microbiol 77(4): 1153-1161.)

Cruises and sampling campaigns:

2017:

1. RV SONNE, Pacific Ocean (SO254)

2016

1. RV Sonne, Pacific Ocean (SO248)

2014

1. RV Heincke, North Sea (HE425)

2012

1. Jyllinge Habour, Jyllinge, Dänemark: Phaeobacter gallaeciensis (Cooparation with project B2 and Lone Gram (DTU))
2. RV Polarstern, ANTXXVII/5: Atlantic transect (Punta Arenas - Bremerhaven)
3. RV Polarstern, ANTXXVII/4: Drake Passage and Southern Ocean (Punta Arenas - Antarktis)
4. RV Meteor, Ausfahrt M86/4: Mediterranean Sea transect (Dubrovnik - Palma de Mallorca)

2011

1. RV Polarstern, ANT-XXVII/2, Southern Ocean (Cape Town - Neumeyer Station)
2. RV Heincke, North Sea (HE361)

2010

1. RV Heincke, North Sea (HE327)

Relevant publications:

2017

1. Dogs M, Wemheuer B, Wolter L, Bergen N, Daniel R, Simon M, Brinkhoff T (2017) Rhodobacteraceae on the marine brown alga Fucus spiralis are predominant and show physiological adaptation to an epiphytic lifestyle. Syst Appl Microbiol, in press (abstract).
2. Ebert M, Laass S, Thürmer A, Roselius L, Eckweiler D, Daniel R, Härtig E and Jahn D (2017) FnrL and three Dnr regulators are used for the metabolic adaptation to low oxygen tension in Dinoroseobacter shibae. Front Microbiol 8:642 (abstract).
3. Schneider D, Wemheuer F, Pfeiffer B, Wemheuer B (2017) Extraction of total DNA and RNA from marine filter samples and generation of a universal cDNA as universal template for marker gene studies. Methods in Molecular Biology 1539:13-22 (abstract).
4. Simon C, Daniel R (2017) Construction of small-insert and large-insert metagenomic libraries. Methods in Molecular Biology 1539:1-12 (abstract).
5. Wöhlbrand L, Wemheuer B, Feenders C, Ruppersberg HS, Hinrichs C, Blasius B, Daniel R, Rabus R (2017a) Complementary metaproteomic approaches to assess the bacterioplankton response toward a phytoplankton spring bloom in the Southern North Sea. Front Microbiol 8:442 (abstract).

2016

1. Billerbeck S, Wemheuer B, Voget S, Poehlein A, Giebel H-A, Brinkhoff T, Gram L, Jeffrey WH, Daniel R, Simon M (2016) Biogeography and environmental genomics of the Roseobacter-affiliated pelagic CHAB-I-5 lineage. Nature Microbiol 1:16063 (abstract).
2. Giebel H-A, Klotz F, Voget S, Poehlein A, Grosser K, Teske A, Brinkhoff T (2016) Draft genome sequence of the marine Rhodobacteraceae strain O3.65, cultivated from oil-polluted seawater of the Deepwater Horizon oil spill. Stand Genomic Sci 11:81 (abstract).
3. Kanukollu S, Wemheuer B, Herber J, Billerbeck S, Lucas J, Daniel R, Simon M, Cypionka H, Engelen B (2016) Distinct compositions of free-living, particle-associated and benthic communities of the Roseobacter group in the North Sea. FEMS Microbiol Ecol 92:fiv137 (abstract).
4. Kanukollu S, Voget S, Pohlner M, Vandieken V, Petersen J, Kyrpides NC, Woyke T, Shapiro N, Göker M, Klenk HP, Cypionka H, Engelen B (2016) Genome sequence of Shimia str. SK013, a representative of the Roseobacter group isolated from marine sediment. Stand Genomic Sci 11:25 (abstract).
5. Osterholz H, Singer G, Wemheuer B, Daniel R, Simon M, Niggemann J, Dittmar T (2016) Deciphering associations between dissolved organic molecules and bacterial communities in a pelagic marine system. ISME J 1-14 (abstract).

2015

1. Aßhauer KP, Wemheuer B, Daniel R, Meinicke P (2015) Tax4Fun: predicting functional profiles from metagenomic 16S rRNA data. Bioinformatics 31:2882-2884 (abstract).
2. Daniel R (2015) Mikrobielle Genomforschung - Schlüsseltechnologie der Lebenswissenschaften. BIOspektrum 21:28-29 (abstract).
3. Gram L, Rasmussen BB, Wemheuer B, Bernbom N, Ng YY, Porsby CH, Breider S, Brinkhoff T (2015) Phaeobacter inhibens from the Roseobacter clade has an environmental niche as a surface colonizer in harbors. Syst Appl Microbiol 38:483-493 (abstract).
4. Neumann AM, Balmonte JP, Berger M, Giebel HA, Arnosti C, Voget S, Simon M, Brinkhoff T, Wietz M (2015) Different utilization of alginate and other algal polysaccharides by marine Alteromonas macleodii ecotypes. Environ Microbiol 17:3857-3868 (abstract).
5. Voget S, Wemheuer B, Brinkhoff T, Vollmers J, Dietrich S, Giebel H.-A., Beardsley C, Sardemann C, Bakenhus I, Billerbeck S, Daniel R, Simon M (2015) Adaptation of an abundant Roseobacter RCA organism to pelagic systems revealed by genomic and transcriptomic analyses. ISME J 9: 371-384 (abstract).
6. Voget S, Valerio SMD, von Hoyningen-Huene AJE, Nattramilarasu PK, Vollheyde K, Xiao S, Daniel R (2015) Genome sequence of Jannaschia aquimarina GSW-M26, a member of the Roseobacter clade. Genome Announc 3:e00353-15 (abstract).
7. Voget S, Billerbeck S, Simon M, Daniel R (2015) Closed genome sequence of Octadecabacter temperatus SB1, the first mesophilic species of the genus Octadecabacter. Genome Announc 3:e01051-15 (abstract).
8. Voget S, Bruns H, Wagner-Döbler I, Schulz S, Daniel R (2015) Draft genome sequence of Roseovarius tolerans EL-164, a producer of N-acylated alanine methyl esters and N-acylhomoserine lactones. Genome Announc 3:e01096-15 (abstract).
9. Wemheuer B, Wemheuer F, Hollensteiner J, Meyer F-D, Voget S, Daniel R (2015) The green impact: bacterioplankton response towards a phytoplankton spring bloom in the southern North Sea assessed by comparative metagenomic and metatranscriptomic approaches. Front Microbiol 6:805 (abstract).
10. Wietz M, Wemheuer B, Simon H, Giebel HA, Seibt MA, Daniel R, Brinkhoff T, Simon M (2015) Bacterial community dynamics during polysaccharide degradation at contrasting sites in the Southern and Atlantic Oceans. Environ Microbiol 17:3822-3831 (abstract).

2014

1. Nacke H, Daniel R (2014) Approaches in metagenome research - progress and challenges. In: Encyclopedia of Metagenomics. SpringerReference (Ed: Nelson, K.). Springer-Verlag Berlin Heidelberg SpringerReference_363415 (abstract).
2. Thürmer A (2014) Next Generation Sequencing in der mikrobiellen (Meta)Genomforschung. BIOspektrum 2.14:168-171 (abstract).
3. Voget S, Göker M, Brinkhoff T (2014) Genomik: Grundlage zum Verständnis des Erfolgs der Roseobacter-Gruppe. BIOspektrum 3.14:279-282 (abstract).
4. Wemheuer B, Güllert S, Billerbeck S, Giebel H-A, Voget S, Simon M, Daniel R (2014) Impact of a phytoplankton bloom on the diversity of the active bacterial community in the southern North Sea as revealed by metatranscriptomic approaches. FEMS Microbiology Ecology 87:378-389 (abstract).

2013

1. Bruns H, Thiel V, Voget S, Patzelt D, Daniel R, Wagner-Döbler I, Schulz S (2013) N-Acylated alanine methyl esters (NAMEs) from Roseovarius tolerans, structural analogs of quorum-sensing autoinducers, N-acylhomoserine lactones. Chemistry & Biodiversity 10:1559-1573 (abstract).
2. Dogs M, Voget S, Teshima H, Petersen J, Davenport K, Dalnigault H, Chen A, Pati A, Ivanova N, Goodwin LA, Chain P, Detter JC, Standfest S, Rohde M, Gronow S, Kyrpides NC, Woyke T, Simon M (2013) Genome sequence of Phaeobacter inhibits type strain (T5T), a secondary metabolite producing member of the marine Roseobacter clade, and emendation of the species description of Phaeobacter inhibits. Stand Genomic Sci 9:142-159.
3. Giebel H-G, Kalhoefer D, Gahl-Janssen R, Choo Y-J, Lee K, Cho J-C, Tindall BJ, Rhiel E, Beardsley C, Aydogmus ÖO, Voget S, Daniel R, Simon M, Brinkhoff T (2013) Planktomarina temperata gen. nov., sp. nov., belonging to the globally distributed RCA cluster of the marine Roseobacter clade, isolated from the German Wadden Sea. Int J Syst Evol Microbiol 63:4207–4217 (abstract).
4. Vollmers J, Voget S, Dietrich S, Gollnow K, Smits M, Meyer K, Brinkhoff T, Simon M, Daniel R (2013) Poles apart: arctic and antarctic Octadecabacter strains share high genome plasticity and a new type of xanthorhodopsin. PLoS One 8:e63422 (abstract).

2012

1. Berger M, Brock N, Liesegang H, Dogs M, Preuth I, Simon M, Dickschat J, Brinkhoff T (2012) Genetic analysis of the upper phenylacetate catabolic pathway in the production of tropodithietic acid by Phaeobacter gallaeciensis. Appl Environ Microbiol 78:3539-51 (abstract).
2. Brinkhoff T, Fischer D, Vollmers J, Voget S, Beardsley C, Thole S, Mussmann M, Kunze B, Wagner-Döbler I, Daniel R, Simon M (2012) Biogeography and phylogenetic diversity of a cluster of exclusively marine myxobacteria. ISME J 6:1260-1272 (abstract).
3. Thole S, Kalhoefer D, Voget S, Berger M, Engelhardt T, Liesegang H, Wollherr A, Kjelleberg S, Daniel R, Simon M, Thomas T, Brinkhoff T (2012) Phaeobacter gallaeciensis genomes from globally opposite locations reveal high similarity of adaptation to surface life. ISME J 6:2229-2244 (abstract).
4. Wemheuer B, Wemheuer F, Daniel R (2012) RNA-based assessment of diversity and composition of active archaeal communities in the German Bight. Archaea 2012: Article ID 695826 (abstract).

2011

1. Kalhoefer D, Thole S, Voget S, Lehmann R, Liesegang H, Wollher A, Daniel R, Simon M, Brinkhoff T (2011) Comparative genome analysis and genome-guided physiological analysis of Roseobacter litoralis. BMC Genomics 12:324 (abstract).
2. Simon C, Daniel R (2011) Metagenomic analyses: past and future trends. Appl Environ Microbiol 77(4):1153-1161 (abstract).

2010

1. Wagner-Döbler I, Ballhausen B, Berger M, Brinkhoff T, Buchholz I, Bunk B, Cypionka H, Daniel R, Drepper T, Gerdts G, Hahnke S, Han C, Jahn D, Kalhoefer D, Kiss H, Klenk HP, Kyrpides N, Liebl W, Liesegang H, Meincke L, Pati A, Petersen J, Piekarski T, Pommerenke C, Pradella S, Pukall R, Rabus R, Stackebrandt E, Thole S, Thompson L, Tielen P, Tomasch J, von Jan M, Wanphrut N, Wichels A, Zech H, Simon M (2010) The complete genome sequence of the algal symbiont Dinoroseobacter shibae: a hitchhiker's guide to life in the sea. ISME J 4(1):61-77 (abstract).
2. Simon C, Daniel R (2010) Construction of small-insert and large-insert metagenomic libraries. Methods in Molecular Biology 668: 39-50

Other Publications

• Beardsley C, 12 co-authors, Simon M (2012) The Roseobacter clade and the dissolved organic matter (DOM) composition in the Atlantic sector of the Southern Ocean. In: Kattner G (ed) The expedition of the Research Vessel "Polarstern" to the Antarctic in 2012 (ANT-XXVIII/2) Reports on Polar and Marine Research 646: 36-39.
• Simon M, and 13 co-authors (2012) In: Bumke K (ed) The expedition of the Research Vessel "Polarstern" to the Antarctic in 2012 (ANT-XXVIII/5) Reports on Polar and Marine Research 654: 30-35.
• Simon, M, and 11 co-authors (2012) Composition and activity of the bacterioplankton communities in the Drake Passage and Antarctic Peninsula region with a special emphasis on the Roseobacter clade and dissolved organic matter. In: Lucassen M (ed) The expedition of the Research Vessel "Polarstern" to the Antarctic in 2012 (ANT-XXVIII/4) Reports on Polar and Marine Research 653: 49-54.

Presentations at national and international symposia (selection)

Talks:

1. Wemheuer B et al. (2016). Driving forces of bacterioplankton community structure, diversity and function in the North Sea. Functional Metagenomics 2016 in Inderøy, Norway
2. Wemheuer et al. (2015). The green impact – bacterioplankton response towards a phytoplankton spring bloom in the southern North Sea assessed by comparative metagenomic and metatranscriptomic approaches. Annual Conference of the Association for General and Applied Microbiology (VAAM) 2015 in Marburg, Germany.
3. Wemheuer B (2013). Metagenomics and metatranscriptomics at the Goettingen Genomics Laboratory. German Conference on Bioinformatics (GCB) 2013 in Goettingen, Germany.

Poster presentations:

1. TBA

Bachelor, Master und PhD theses:

Running

1. Florian Lenk (PhD thesis)

2017

1. Avril von Hoyningen-Huene (Master): "Structural and functional characterization of microbial communities in the ocean"

2016

1. Pinar Akyol (Master): "Bacterioplankton community structures and functions along geographical gradients in the North Sea"
2. Dirk Berkelmann (Master): "From order to chaos – bacterial community dynamics under different environmental regimes in a simulated marine ecosystem"

2015

1. Ines Friedrich (Bachelor): "Development of novel Escherichia coli mutants for funtional screenings of metagenomic libraries."
2. Katharina Smaluch (Master): "Impact of phytoplankton blooms and other environmental parameterson bacterioplankton communities
3. Carl Simon Strittmatter (Bachelor): "Characterization of metagenomes derived from aquatic habitats"

2014

1. Bernd Wemheuer (PhD): "Diversity, ecology and physiology of the Roseobacter clade and other marine microorganisms in the North Sea as revealed by culture-independent approaches"

2013

1. Peggy Klempert (Diplom): "Characterization of marine microbial communites applying culture-indipendent appraoches"
2. Florian Lenk (Master): "Metagenomic analysis of antarctic se ice samples"
3. John Vollmers (PhD): "Genomic comparisation and molecular characterization of selected members of the Roseobacter-clade"

2012

1. Simon Güllert (Master): "Phylogenetic and functional characterization of microbial communities derived from the German Bight"
2. Dimitri Meier (Master): "Phylogenetic and functional characterization of microbial communities derived from the North Sea along a North-South gradient from Germany to Norway"
3. Katja Meyer (Master): "Distribution and Function of selected Rhodopsin Families"

2011

1. Pinar Akyol (Bachelor): "Purification and Characterization of a metagenome-derived Peptidase"
2. Maike Smits (Bachelor): "Functional and comparative Analyses of Rhodopsins from selected polar Roseobacter strains"

Contact

Address

Georg-August University Göttingen
Institute of Microbiology and Genetics
Department of Genomic and Applied Microbiology and Göttingen Genomics Labratory
Grisebachstr. 8, 37077 Göttingen, Germany

eMail                                rdaniel(at)gwdg.de

Phone                            +49 (0)551 39-33827

Phone (Secratary)          +49 (0)551 39-33842

Fax                                   +49 (0)551 39-1218

URL                                    http://appmibio.uni-goettingen.de/

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Extrachromosomal, extraordinary and essential – the mobilome of the Roseobacter group

The Roseobacter ‘plasmid’ team 2017:

Principal investigators: PD Dr. Jörn Petersen, Dr. Silke Pradella

Research Associate: Dr. Henner Brinkmann

PhD student: Pascal Bartling

Technical assistance: Claire Ellebrandt, Victoria Michael, Orsola Päuker

Master students: Lukas Birmes, Sandra Hacke

 From left to right: Victoria, Jörn, Claire, Silke, Sandra, Pascal, Orsola, Henner, Lukas

Introduction

Research in our team is focused on the evolution and function of extrachromosomal replicons (ECRs or ‘plasmids’), which are highly abundant in Roseobacter genomes.

As other Alphaproteobacteria typical representatives of the Roseobacter group own multipartite genomes. These are composed of a single chromosome and a variable number of ECRs. For example, twelve ECRs were detected in the Roseobacter species Marinovum algicola. This number is even unsurpassed within the Proteobacteria and the ECRs of this species account for about one-third of the total genomic information. Important functions have been assigned to Roseobacter plasmids, including aerobic anoxygenic photosynthesis (Fig. 1), motility, biofilm formation and synthesis of the antibiotic tropodithietic acid (TDA). It is hypothesized that ECRs mediate the horizontal gene transfer of privotal functions and might thus allow to the rapid adaptions of roseobacters to changing environments.

Due to the conspicuous wealth of Roseobacter ECRs and the availability of an exceptional amount of genome data (> 450 Rhodobacteraceae genomes have been sequenced [01/2017]) the Roseobacter group constitutes an ideal platform for the investigation of alphaproteobacterial plasmids.

Fig. 1 Pink is beautiful! The characteristic pink color of aerobic anoxygenic photosynthetic members of the Roseobacter clade is caused by photosynthetic pigments (carotenoids). The Erlenmeyer flask shown here contains a culture of Dinoroseobacter shibae DSM 16493 representing the photosynthetic model organism of the collaborative research center (CRC) 51. In contrast to Roseobacter litoralis and Sulfitobacter guttiformis, the 45 kb photosynthetic gene cluster is chromosomally encoded in this strain (Wagner-Döbler et al. 2010).

As main goals of our project A5 we aim to reveal:

1.  Evolutionary aspects

• Plasmid abundance, distribution and relevance in the Roseobacter group

• A natural classification scheme for Roseobacter plasmids based on the phylogeny of plasmid replication and partitioning genes

• The genetic basis for compatibility and the host-range of alphaproteobacterial plasmids

• The role of the extrachromosomal replicons ECRs in the dynamics of Roseobacter genomes

2.  Functional aspects

• The functional consequences of plasmid loss (via curing) or plasmid gain (via conjugation) in Roseobacter strains

• The role of ECRs in symbiotic associations of roseobacters with marine micro- and macroalgae

Outcome (2010-2017)

1.  Genomics of roseobacters

1.1  Think Pink! – Complete photosynthesis gene clusters are plasmid-encoded!

• As a highlight of the first funding period we showed that a complete photosynthesis gene cluster (45 kb) is located on the 118 kb plasmid of Sulfitobacter guttiformis^T (Fig. 2) and hypothesized that the horizontal gene transfer of extrachromosomal replicons drives evolution in the Roseobacter group.

Fig. 2. Comparison of plasmid-located PGCs from Sulfitobacter guttiformis and Roseobacter litoralis with chromosomal counterparts from Roseobacter denitrificans and Rhodobacter sphaeroides.

1.2  Genome sequencing of plasmid-rich roseobacters (Rhodobacteraceae) and relatives

• Dinoroseobacter shibae DSM 16493^T: 5 plasmids (72 to 191 kb; in cooperation with project B4; Wagner-Döbler et al. 2010)

• Marinovum algicola DG898 (DSM 27768): 11 plasmids (6 to 255 kb, Pradella et al. 2010). We completely sequenced the genome of this strain in order to understand the molecular basis for maintaining a multipartite genome organization (Frank et al. 2015a; Fig. 3).

• Phaeobacter gallaeciensis DSM 26640^T: 7 plasmids (40 to 255 kb; Frank et al. 2015b; Buddruhs & Pradella et al. 2013)

• Others: Shimia str. SK013 (Kanukollu et al. 2016), Loktanella hongkongensis^T (Lau et al. 2015), Roseovarius mucosus^T (Riedel et al. 2015), Rubellimicrobium mesophilum^T (Riedel et al. 2014), Wenxinia marina^T (Riedel et al. 2014), Salipiger mucosus^T (Riedel et al. 2014), Hoeflea phototrophica^T (Fiebig et al. 2013b), Labrenzia alexandrii^T (Fiebig et al. 2013a)

Fig. 3. Ocean’s Twelve: Circular maps of the chromosome and 11 extrachromosomal replicons (ECR) of Marinovum algicola DG898 (DSM 27768). The ECR account for more than 30 % of the genome!

2.  Classification and compatibility of plasmids in the Roseobacter group

• We developed a robust classification scheme for Roseobacter plasmids based on the phylogeny of the plasmidal replicase and partitioning genes (Petersen et al. 2009, Petersen 2011). Our phylogenetic plasmid data base is continuously updated with incoming Roseobacter genome sequences.

• On basis of the thitherto unknown DnaA-like replicase a novel plasmid-type was identified in Rhodobacterales (Petersen et al. 2011).

• Our phylogeny-based plasmid classification allowed predictions about the plasmid compatibility and was a prerequisite to develop a target-orientated plasmid curing strategy (see below; Petersen et al. 2011).

3.  Target-orientated plasmid curing to reveal plasmid functions

In order to reveal the function of specific plasmids, we designed a target-oriented plasmid curing strategy for Roseobacter strains (Petersen et al. 2013). Various cured Roseobacter plasmid mutants, including mutants of CRC 51 model strains, were generated:

• Phaeobacter inhibens DSM 17395 (3 native plasmids): The complete set of mutants cured from all native plasmids in every combination was obtained (Trautwein et al. 2016).

• Dinoroseobacter shibae DFL-12 (5 plasmids): 3 plasmid mutants - Δ191 kb, Δ86 kb, Δ72 kb

• Other mutans derived from: Marinovum algicola DG898 (DSM 27768; Frank et al 2015a), Marinovum algicola DSM10251^T, Phaeobacter inhibens DSM 24588, Phaeobacter gallaeciensis DSM 26640^T, Pseudophaeobacter arcticus DSM 23566^T (Michael et al. 2016)

4.  Essential functions of ECRs demonstrated by target-orientated plasmid curing

Roseobacter wildtype strains and the corresponding plasmid mutants were compared in the laboratory experiments and the “loss of function” of the mutant strain was revealed.

   Dinoroseobacter shibae DFL-12^T:

• The 191 kb “killer” plasmid is essential for the anaerobic growth of D. shibae DFL-12 (Ebert et al. 2013) and cell density dependent killing effect of this strain on the dinoflagellate Prorocentrum minimum (in cooperation with project B4; Wang et al. 2015).

• The 72 kb plasmid is pivotal for adaptation to starvation and oxidative stress (in cooperation with project B1; Soora et al. 2015).

   Phaeobacter inhinbens DSM 17395:

• The 65 kb plasmid is required for biofilm formation, motility and colonization of marine algae (Frank et al. 2015b, Fig. 4). Biofilm plasmids of this type are widely distributed among the Roseobacter group and are essential for the sessile mode of life in many of these strains (Michael et al. 2016).

Fig. 4 Phaeobacter inhibens DSM 17395 colonizes the surface of the axenic dinoflagellate Prorocentrum minimum CCMP 1329 when co-cultivated. The scanning electron micrograph was taken by Manfred Rohde (Frank et al. 2015b).

• Systems biology of the Phaeobacter inhibens DSM 17395 plasmid mutants. Based on the complete set of plasmid curing mutants derived from Phaeobacter inhibens DSM 17395, the physiological and energetic consequences of plasmid carriage were investigated. Maintenance of the large TDA-encoding 262 kb plasmid was shown to be extremely costly for our model strain Phaeobacter inhibens DSM 17395 (in cooperation with projects C1 and C3; Trautwein et al. 2016)!

   Marinovum algicola DG 898:

• The 52 kb plasmid represented a biofilm plasmid and is required for surface attachment (Frank et al. 2015a).

• A complete flagellum gene cluster is located on the 143 kb plasmid of strain DG898. In contrast to the wildtype, the cured plasmid mutant D143 kb is immotile (Frank et al. 2015a).

5.  Conjugation

• The conjugative transfer of ECRs between Dinoroseobacter shibae DFL-12 as donor and Phaeobacter inhibens DSM 17395 as recipient was proven (in cooperation with project B4; Patzelt et al. 2016; Fig. 5).

Fig. 5 Interspecies conjugation of two plasmids from Dinoroseobacter shibae DFL-12 (Dshi) into Phaeobacter inhibens DSM 17395 (Phaeo). Transferred plasmids are indicated with red stars. WT, wild type; TK, transconjugant; Chr, chromosome (Patzelt et al. 2016).

6.  Transposon mutagenesis

• A transoposon library of Phaeobacter inhibens DSM 17395 containing 5500 quality checked mutants was established.

Current projects

• Plasmid transfer between roseobacters and rhizobia: We determine the host range of RepABC-type plasmids.

• Detection of novel DnaA-like I photosynthesis plasmids

• Evolution of photosynthesis in Rhodobacteraceae

• Identification of a novel promiscuous plasmid type RepL in roseobacters

• Comparative genomics of Marinovum algicola strains. We compare the genome sequences of the closely related Marinovum algicola strains in order to reveal the genome dynamics in this plasmid-rich species (in cooperation with projects A6 and A7).

• Plasmid flux and horizontal gene transfer in the genus of Phaeobacter (in cooperation with project A7)

• Dinoroseobacter shibae DFL-12 – The sixth element. Pulsed-field gel electrophoresis analyses of different glycerol stock cultures showed that our completely sequenced model organism D. shibae DSM 16493^T lost two plasmids in the course of cryoconservation. We isolated and sequenced a sixth plasmid of Dinoroseobacter shibae DFL-12 (in cooperation with project A3). The 102 kb replicon is dominated by genes that assumingly confer resistance to a broad spectrum of heavy metals. We performed several physiological tests to differentiate between the two D. shibae plasmid mutants and determine the gene expression of the sixth element by comparative transcriptome analysis.

• The archaetypal type I flagellar system of Rhodobacteraceae. The three flagellar systems of Rhodobacteraceae are analyzed.

• Bacterial communities in non-axenic algal cultures. We analyze the composition of the bacterial communities associated with 23 xenic algae cultures from marine and brackish environments. Culture-independent methods, i.e. barcoded partial 16S rRNA gene 454-pyrosequencing and cultivation are used in order to quantify the amount of the bacterial epibionts and to reveal specific associations (in cooperation with project A3).

• Algal tumors of the red alga Ceramium rubrum: Are roseobacters involed in the gall formation? The bacterial community of algal galls is analyzed by culture- independent and -dependent methods.

Methods

• Cultivation, isolation and characterization of bacteria
• Cultivation of microalgae
• Broad spectrum of molecular methods (DNA and RNA isolation, PCR, cloning, hybridization)
• Pulsed-field gel electrophoresis for Roseobacter genome structure analyses
• Target-orientated plasmid curing to generate plasmid mutants
• Transposon Mutagenesis
• Next generation sequencing and genome finishing (Illumina, PacBio)
• Transcriptome analyses using the Illumina technology
• Phylogenetic and phylogenomic analyses
• Comparative genomics
• Phenotype MicroArray technology (Biolog)
• Bacterial community analysis of xenic algal cultures using 16S rDNA amplicon sequencing

International Cooperations

• Baurain Denis, Université of Liège, Liège, Belgium
• Gram Lone, TU Denmark, Lyngby, Denmark
• Green David, Scottish Marine Institute, Oban, UK
• Jogler Christian, Radboud University, Nijmegen, The Netherlands
• Kaster Anne-Kristin, DSMZ Braunschweig, Germany
• Klenk Hans-Peter, Newcastle University, UK
• Kolter Roberto, Harvard Medical School, Boston, USA
• Philippe Hervé, CNRS Moulis, France
• Santini Joanne, University College London, UK
• Segev Einat, Harvard Medical School, Boston, USA
• Summers Anne, University of Georgia, USA
• Wichard Thomas, Uni Jena, Germany

Publications

Second funding period (2014-2017)

• Bartling P, Brinkmann H, Bunk B, Overmann J, Göker M, Petersen J (2017). The composite 259-kb plasmid of Martelella mediterranea DSM 17316T – A natural replicon with functional RepABC modules from Rhodobacteraceae and Rhizobiaceae. Front Microbiol in press (DOI: 10.3389/fmicb.2017.01787).
• Dickschat J, Rinkel J, Klapschinski T, Petersen J (2017). Characterisation of the L-cystine b-lyase PatB from Phaeobacter inhibens, an enzyme involved in the biosynthesis of the marine antibiotic tropodithietic acid. ChemBioChem in press (DOI:10.1002/cbic.201700358).
• Petersen J, Wagner-Döbler I (2017). Plasmid transfer in the ocean - a case study from the Roseobacter group. Front Microbiol: 8: 1350 (DOI: 10.3389/fmicb.2017.01350).
• Simon M, Scheuner C, Meier-Kolthoff JP, Brinkhoff T, Wagner-Döbler I, Ulbrich M, Klenk HP, Schomburg D, Petersen J, Göker M. (2017). Phylogenomics of Rhodobacteraceae reveals evolutionary adaptation to marine and non-marine habitats. ISME J 11: 1483-1499 (DOI: 10.1038/ismej.2016.198).
• Will SE, Neumann-Schaal M, Heydorn RL, Bartling P, Petersen J, Schomburg D (2017). The limits to growth – energetic burden of the endogenous tropodithietic acid in Phaeobacter inhibens DSM 17395. PLoS ONE 12: e0177295 (DOI: 10.1371/journal.pone.0177295).
• Segev E, Wyche TP, Kim KH, Petersen J, Ellebrandt C, Vlamakis H, Barteneva N, Pauson JN, Chai L, Clardy J, Kolter R (2016). Dynamic metabolic exchange governs a marine algal-bacterial interaction. eLife 5: e17473 (DOI: 10.7554/eLife.17473).
• Michael V, Frank O, Bartling P, Scheuner C, Göker M, Brinkmann H, Petersen J (2016). Biofilm plasmids with a rhamnose operon are widely distributed determinants of the “swim-or-stick” lifestyle in roseobacters. ISME J 10: 2498-2513 (DOI: 10.1038/ismej.2016.30).
• Trautwein K, Will SE, Hulsch R, Maschmann U, Wiegmann K, Hensler M, Michael V, Ruppersberg H, Wünsch D, Feenders C, Neumann-Schaal M, Kaltenhäuser S, Ulbrich M, Schmidt-Hohagen K, Blasius B, Petersen J, Schomburg D, Rabus R (2016). Native plasmids restrict growth of Phaeobacter inhibens DSM 17395. Energetic costs of plasmids assessed by quantitative physiological analyses. Environ Microbiol 18: 4817- 4829 (DOI: 10.1111/1462-2920.13381).
• Patzelt D, Michael V, Päuker O, Ebert M, Tielen P, Jahn D, Tomasch J, Petersen J, Wagner-Döbler I (2016). Gene flow across genus barriers - conjugation of Dinoroseobacter shibae’s 191-kb killer plasmid into Phaeobacter inhibens and AHL-mediated expression of type IV secretion systems. Front Microbiol 7: 742 (DOI: 10.3389/fmicb.2016.00742).
• Kanukollu S, Voget S, Pohlner M, Vandieken V, Petersen J, Kyrpides NC, Woyke T, Shapiro N, Göker M, Klenk H, Cypionka H, Engelen B (2016). Genome sequence of Shimia str. SK013, a representative of the Roseobacter group isolated from marine sediment. Stand Genomic Sci 11: 25 (DOI: 10.1186/s40793-016-0143-0).
• Wang H, Tomasch J, Michael V, Bhuju S, Jarek M, Petersen J, Wagner-Döbler I (2015). Identification of genetic modules mediating the Jekyll and Hyde interaction of Dinoroseobacter shibae with the dinoflagellate Prorocentrum minimum. Front Microbiol 6: 1262 (DOI: 10.3389/fmicb.2015.01262).
• Frank O, Göker M, Pradella S, Petersen J (2015). Ocean’s Twelve: flagellar and biofilm chromids in the multipartite genome of Marinovum algicola DG898 exemplify functional compartmentalization. Environ Microbiol 17: 4019–4034 (DOI: 10.1111/1462-2920.12947).
• Lau CKS, Riedel T, Fiebig A, Han J, Huntemann M, Petersen J, Ivanova NN, Markowitz V, Woyke T, Göker M, Kyrpides NC, Klenk H-P, Qian P-Y (2015). Genome sequence of the pink-pigmented marine bacterium Loktanella hongkongensis type strain (UST950701-009PT), a representative of the Roseobacter group. Stand Genomic Sci 10: 51 (DOI: 10.1186/s40793-015-0050-9).
• Soora M, Tomasch J, Wang H, Michael V, Petersen J, Engelen B, Wagner-Döbler I, Cypionka H (2015). Oxidative stress and starvation in Dinoroseobacter shibae: The role of extrachromosomal elements. Front Microbiol 6: 233 (DOI: 10.3389/fmicb.2015.00233).
• Frank O, Michael V, Päuker O, Boedeker C, Jogler C, Rohde M, Petersen J (2015). Plasmid curing and the loss of grip - The 65-kb replicon of Phaeobacter inhibens DSM 17395 is required for biofilm formation, motility and the colonization of marine algae. Syst Appl Microbiol 38: 120–127 (DOI: 10.1016/j.syapm.2014.12.001).
• Riedel T, Spring S, Fiebig A, Scheuner C, Petersen J, Göker M (2015). Genome sequence of the Roseovarius mucosus type strain (DSM 17069^T), a bacteriochlorophyll a-containing representative of the marine Roseobacter group isolated from the dinoflagellate Alexandrium ostenfeldii. Stand Genomic Sci 10: 17 (DOI: 10.1186/1944-3277-10-17).
• Breider S, Scheuner C, Schumann P, Fiebig A, Petersen J, Pradella S, Klenk H-P, Brinkhoff T, Göker M (2014). Genome-scale data suggest reclassifications in the Leisingera-Phaeobacter cluster including proposals for Sedimentitalea gen. nov. and Pseudophaeobacter gen. nov. Front Microbiol 5: 416 (DOI: 10.3389/fmicb.2014.00416).
• Breider S, Teshima H, Petersen J, Fiebig A, Chertkov O, Dalingault H, Chen A, Pati A, Goodwin LA, Chain P, Detter JC, Ivanova NN, Lapidus A, Rohde M, Tindall BJ, Kyrpides NC, Woyke T, Simon M, Göker M, Klenk HP, Brinkhoff T (2014) Complete genome sequence of Leisingera nanhaiensis strain DSM 24252^T isolated from marine sediment. Stand Genomic Sci 9: 687-703 (DOI: 10.4056/sigs.3828824).
• Petersen J, Ludewig AK, Michael V, Bunk B, Jarek M, Baurain D, Brinkmann H (2014). Chromera velia, endosymbioses and the rhodoplex hypothesis - plastid evolution in cryptophytes, alveolates, stramenopiles, and haptophytes (CASH lineages). Genome Biol Evol 6: 666–684 (DOI: 10.1093/gbe/evu043).
• Wang H, Ziesche L, Frank O, Michael V, Martin M, Petersen J, Schulz S, Wagner-Döbler I, Tomasch J (2014). The CtrA phosphorelay integrates differentiation and communication in the marine alphaproteobacterium Dinoroseobacter shibae. BMC Genomics 15: 130 (DOI: 10.1186/1471-2164-15-130).
• Frank O, Pradella S, Rohde M, Scheuner C, Klenk H-P, Göker M, Petersen J (2014). Complete genome sequence of the Phaeobacter gallaeciensis type strain CIP 105210^T (= DSM 26640^T = BS107^T). Stand Genomic Sci 9: 914–932 (DOI: 10.4056/sigs.5179110).
• Riedel T, Spring S, Fiebig A, Petersen J, Göker M, Klenk H-P (2014). Genome sequence of the pink to light reddish-pigmented Rubellimicrobium mesophilum type strain (DSM 19309^T), a representative of the Roseobacter group isolated from soil, and emended description of the species. Stand Genomic Sci 9: 902–913 (DOI: 10.4056/sigs.5621012).
• Riedel T, Fiebig A, Han J, Huntemann M, Spring S, Petersen J, Ivanova NN, Markowitz V, Woyke T, Göker M, Kyrpides NC, Klenk H-P (2014). Genome sequence of the Wenxinia marina type strain (DSM 24838^T), a representative of the Roseobacter group isolated from oilfield sediments. Stand Genomic Sci 9: 855–865 (DOI: 10.4056/sigs.5601028).
• Riedel T, Spring S, Fiebig A, Petersen J, Kyrpides NC, Göker M, Klenk H-P (2014). Genome sequence of the exopolysaccharide-producing Salipiger mucosus type strain (DSM 16094^T), a moderately halophilic member of the Roseobacter clade. Stand Genomic Sci 9: 1331–1343 (DOI: 10.4056/sigs.4909790).

First funding period (2010-2013)

• Buddruhs N*, Pradella S*, Göker M, Päuker O, Pukall R, Spröer C, Schumann P, Petersen J, Brinkhoff T (2013). Molecular and phenotypic analyses reveal the non-identity of the Phaeobacter gallaeciensis type strain deposits CIP 105210^T and DSM 17395. Int J Syst Evol Microbiol 63: 4340-4349. (*contributed equally) (DOI: 10.1099/ijs.0.053900-0).
• Buddruhs N, Chertkov O, Fiebig A, Petersen J, 10 co-authors, Göker M, Brinkhoff T, Klenk HP (2013). Complete genome sequence of the marine methyl-halide oxidizing Leisingera methylohalidivorans type strain (DSM 14336^T), a member of the Roseobacter clade. Stand Genomic Sci 9:128-41 (DOI: 10.4056/sigs.4297965).
• Brock NL, Citron CA, Zell C, Berger M, Wagner-Döbler I, Petersen J, Brinkhoff T, Simon M, Dickschat JS (2013). Isotopically labeled sulfur compounds and synthetic selenium and tellurium analogs to study sulfur metabolism in marine bacteria. Beilstein J Org Chem 9: 942–950 (DOI: 10.3762/bjoc.9.108).
• Beyersmann PG, Chertkov O, Petersen J, Fiebig A, 11 co-authors, Simon M, Göker M, Klenk HP, Brinkhoff T (2013). Genome sequence of Phaeobacter caeruleus type strain (DSM 24564^T), a surface-associated member of the marine Roseobacter clade. Stand Genomic Sci 8: 403-419 (DOI: 10.4056/sigs.3927626).
• Dogs M, Teshima H, Petersen J, Fiebig A, 13 co-authors, Simon M, Klenk HP, Göker M, Brinkhoff T (2013). Genome sequence of Phaeobacter daeponensis type strain (DSM 23529^T), a facultatively anaerobic bacterium isolated from marine sediment, and emendation of Phaeobacter daeponensis. Stand Genomic Sci 9: 9:9010142 (DOI: 10.4056/sigs.4287962)
• Dogs M, Voget S, Teshima H, Petersen J, Fiebig A, 12 co-authors, Simon M, Klenk HP, Göker M, Brinkhoff T (2013). Genome sequence of Phaeobacter inhibens type strain (T5^T), a secondary-metabolite producing member of the marine Roseobacter clade, and emendation of the species Phaeobacter inhibens. Stand Genomic Sci 9: 334-350 (DOI: 10.4056/sigs.4448212).
• Ebert M, Laaß S, Burghartz M, Petersen J, Koßmehl S, Wöhlbrand L, Rabus R, Wittmann C, Tielen P, Jahn D (2013). Transposon mutagenesis identified chromosomal and plasmid genes essential for adaptation of the marine bacterium Dinoroseobacter shibae to anaerobic conditions. J Bacteriol 195: 4769-4777 (DOI: 10.1128/JB.00860-13).
• Fiebig A, Pradella S, Petersen J, Päuker O, Michael V, Lünsdorf H, Göker M, Klenk H-P, Wagner-Döbler I (2013). Genome of the R-body producing marine alphaproteobacterium Labrenzia alexandrii type strain (DFL-11^T). Stand Genomic Sci 7: 413-426 (DOI: 10.4056/sigs.3456959).
• Fiebig A, Pradella S, Petersen J, Michael V, Päuker O, Rohde M, Göker M, Klenk H-P, Wagner-Döbler I (2013). Genome of the marine alphaproteobacterium Hoeflea phototrophica type strain (DFL-43^T). Stand Genomic Sci 7: 440-448 (DOI: 10.4056/sigs.3486982).
• Freese H, Dalingault H, Petersen J, Pradella S, Fiebig A, 12 co-authors, Brinkhoff T, Göker M, Overmann J, Klenk HP (2013). Genome sequence of the phage-gene rich marine Phaeobacter arcticus type strain DSM 23566^T. Stand Genomic Sci 8: 450–464 (DOI: 10.4056/sigs.383362).
• Patzelt D, Wang, H, Buchholz, I, Rohde, M, Gröbe, L, Pradella S, Neumann A, Schulz S, Heyber S, Muench K, Muench R, Jahn D, Wagner-Döbler I, Tomasch J (2013). You Are What You Talk: Quorum Sensing Induces Individual Morphologies and Cell Division Modes in Dinoroseobacter Shibae. ISME J 7/12: 2274-2286 (DOI: 10.1038/ismej.2013.107).
• Petersen J, Frank O, Göker M, Pradella S (2013). Extrachromosomal, extraordinary and essential - the plasmids of the Roseobacter clade. Appl Microbiol Biotechnol 97: 2805-2815 (DOI: 10.1007/s00253-013-4746-8).
• Riedel T, Fiebig A, Petersen J, Gronow S, Göker M, Klenk HP (2013). Genome sequence of the Litoreibacter arenae type strain (DSM 19593^T), a member of the Roseobacter clade isolated from sea sand. Stand Genomic Sci 9: 117–127.
• Riedel T, Teshima H, Petersen J, Fiebig A, 16 co-authors, Göker M, Brinkhoff T, Klenk HP (2013). Genome sequence of the Leisingera aquimarina type strain (DSM 24565^T), a member of the marine Roseobacter clade rich in extrachromosomal elements. Stand Genomic Sci 8: 389-402 (DOI: 10.4056/sigs.3858183).
• Petersen J, Brinkmann H, Bunk B, Michael V, Päuker O, Pradella S (2012). Think pink: photosynthesis, plasmids and the Roseobacter clade. Environ Microbiol 14: 2661-2672 (DOI: 10.1111/j.1462-2920.2012.02806.x).
• Petersen J, Brinkmann H, Berger M, Brinkhoff T, Päuker O, Pradella S (2011). Origin and evolution of a novel DnaA-like plasmid replication type in Rhodobacterales. Mol Biol Evol 28: 1229-1240 (DOI: 10.1093/molbev/msq310).
• Petersen J (2011). Phylogeny and compatibility: plasmid classification in the genomics era. Arch Microbiol 193: 313-321 (DOI: 10.1007/s00203-011-0686-9).
• Wagner-Döbler I, Ballhausen B, Berger M,..., Petersen J, ..., Pradella S, et al. (2010). The complete genome sequence of the algal symbiont Dinoroseobacter shibae: a hitchhiker's guide to life in the sea. ISME J 4: 61-77 (DOI: 10.1038/ismej.2009.94).
• Pradella S, Päuker O, Petersen J (2010). Genome organisation of the marine Roseobacter clade member Marinovum algicola. Arch Microbiol 192: 115-126 (DOI: 10.1007/s00203-009-0535-2).

Relevant previous work

• Petersen J, Brinkmann H, Pradella S (2009). Diversity and evolution of repABC type plasmids in Rhodobacterales. Environ Microbiol 11: 2627-2638 (DOI: 10.1111/j.1462-2920.2009.01987.x).
• Pradella S, Allgaier M, Hoch C, Päuker O, Stackebrandt E, Wagner-Döbler I (2004). Genome organization and localization of the pufLM genes of the photosynthesis reaction center in phylogenetically diverse marine Alphaproteobacteria. Appl Environ Microbiol 70: 3360-3369 DOI: 10.1128/AEM.70.6.3360-3369.2004).

Contributions to symposia and seminars

Second funding period (2014-2017)

• Petersen J (2017). Foreign affairs – Plasmid transfer between bacterial genera reprograms the gene expression of the new host. Colloquium, 13. June 2017, Nijmegen, Netherlands (talk).
• Petersen J (2017). Foreign affairs – Plasmid transfer between bacterial genera reprograms the gene expression of the new host. BAGECO 14, Bacterial Genetics and Ecology, 4-8 June 2017, Aberdeen, Scotland (talk).
• Bartling P, Bunk B, Overmann J, Brinkmann H, Petersen, J (2017). Foreign affairs: Plasmid transfer between roseobacters and rhizobia. 5^th Joint Conference of the DGHM & VAAM. VAAM Annual Meeting 2017 and 69^th Annual Meeting of the DGHM, Würzburg, Germany, March 05-07.
• Petersen J (2016). Microbial ecology from a plasmid perspective. Harvard Medical School, Boston, USA, October 07^th (talk).
• Petersen J. (2016). Verknüpfung von Grundlagenforschung und Sammlungsaktivität am Beispiel der Roseobacter-Gruppe. Scientist‘s Meeting at DSMZ, Braunschweig, Germany, August 22^th.
• Petersen J (2016). Evolutionary plug and play-plasmid-mediated horizontal transfer of photosynthesis in Rhodobacteraceae. Workshop: Photosynthesis: plug and play? Leiden, The Netherlands, August 15-18 (invited talk).
• Petersen J (2016). Highlights beyond plasmids. 12^th Status Seminar of the CRC 51, Oldenburg, Germany, June 23-24 (talk).
• Petersen J (2016). Extrachromosomal, extraordinary and essential - the mobilome of the Roseobacter group. 12^th Status Seminar of the CRC 51, Oldenburg, Germany, June 23-24 (talk).
• Brinkmann H, Petersen J (2016). RpoB-phylogeny of genome-sequenced Rhodobacteraceae. 12^th Status Seminar of the CRC 51, Oldenburg, Germany, June 23-24 (poster).
• Pradella S, Wemheuer B, Päuker O, Frank O, Daniel R, Petersen J (2016). The bacterial diversity of the phycosphere. Annual Meeting of the German Society of General and Applied Microbiology (VAAM), Jena, Germany, March 13-16 (poster).
• Bartling P, Ellebrandt C, Petersen J (2016). Swimming motility of Phaeobacter inhibens DSM 17395 and the regulation of the archetypal flagellum of Rhodobacteraceae. Annual Meeting of the German Society of General and Applied Microbiology (VAAM), Jena, Germany, March 13-16 (poster).
• Petersen J. (2015). Dinoroseobacter shibae - a genetic nightmare? 11^th Status Seminar of the CRC 51, Braunschweig, Germany, December 9^th (talk).
• Pradella S, Michael V, Ellebrandt C, Päuker O, Bartling P, Frank O, Müller S, Brinkmann H, Petersen J (2015). Significance of plasmids in the Roseobacter group. 11^th Status Seminar of the CRC 51, Braunschweig, Germany, December 9^th (poster).
• Frank O, Göker M, Pradella S, Petersen J (2015). Oceans´s twelve: Flagellar and biofilm chromids in the multipartite genome of Marinovum algicola DG898. Prokkagenomics 2015. 6^th European Conference on Procaryotic an Fungal Genomics, Göttingen, Germany, September 29^th-October 2^nd (poster).
• Pradella S (2015). Oceans´s twelve: Flagellar and biofilm chromids in the multipartite genome of Marinovum algicola DG898. 10^th Status Seminar of the CRC 51, Oldenburg, Germany, May 8^th (talk).
• Petersen J, Bartling P (2015). Transposon mutants of Phaeobacter inhibens DSM 17395. 10^th Status Seminar of the CRC 51, Oldenburg, Germany, May 8^th (talk).
• Petersen J (2015). The sixth element – a 102-kb plasmid of Dinoroseobacter shibae modulates chromosomal gene expression. Annual Meeting of the German Society of General and Applied Microbiology (VAAM), Marburg/Lahn, Germany, March 1-4 (talk).
• Müller S, Hahnke RL, Tegtmeyer HE, Moosmann P, Petersen J, Erb TJ, Strous M (2015). Paracoccus denitrificans and nitrite: 500 generations – problem solved. Annual Meeting of the German Society of General and Applied Microbiology (VAAM), Marburg/Lahn, Germany, March 1-4 (talk).
• Petersen J (2015). One, two, three - Plasmid Curing in Phaeobacter inhibens. Microbiological Seminar at the Institute for Chemistry and Biology of the Marine Environment (ICBM), Oldenburg, Germany, January 21^th (talk).
• Petersen J (2014). Generation of 4,000 Transposon Mutants from Phaeobacter inhibens DSM 17395. 9^th Status Seminar of the CRC 51, Braunschweig, Germany, November 20^th (talk).
• Petersen J (2014). The Sixth Element: The 102-kb Plasmid of Dinoroseobacter shibae modulates chromosomal gene expression. 9^th Status Seminar of the CRC 51, Braunschweig, Germany, November 20^th (talk).
• Petersen J (2014). Plasmid curing and the loss of grip – RepA-I type replicons of the Roseobacter group are essential for biofilm formation, motility and the colonization of marine algae. Annual Meeting of the German Society of General and Applied Microbiology (VAAM), Dresden, Germany, October 05-08 (talk).
• Michael V, Päuker O, Sikorski J, Pradella S, Petersen J (2014). So much more than a souvenir - The relevance of plasmids in roseobacters exemplified for Phaeobacter inhibens DSM 17395. Annual Meeting of the German Society of General and Applied Microbiology (VAAM), Dresden, Germany, October 05-08 (poster).
• Petersen J (2014). Chromera velia, endosymbioses and the rhodoplex hypothesis. XVI. Annual Meeting of the International Society of Endocytobiology German Section (ISE-G). Herzogenhorn, Germany, July 21-24 (talk).
• Ludewig A-K (2014). Apicomplexans and the fate of plastids. XVI. Annual Meeting of the International Society of Endocytobiology German Section (ISE-G). Herzogenhorn, Germany, July 21-24 (talk).
• Petersen J (2014). From malaria to sparkling of the sea - Evolution of complex algae and alveolates. Symposium: Photosynthesis as we don't know it. Düsseldorf, Germany, March 27^th (talk).
• Petersen J (2014). Photosynthesis and plasmid-mediated horizontal gene transfer among roseobacters. Liège, Belgium, February 19^th (talk).
• Brinkmann H (2014). Origin and spread of photosynthesis in proteobacteria. Liège, Belgium, February 19^th (talk).
• Ludewig A-K (2014). Chromerids- connecting link in alveolate evolution. Liège, Belgium, February 19^th (talk).

First funding period (2010-2013)

• Frank O (2013). The plasmid wealth of Marinovum algicola opens new perspectives on multipartite genomes. International Symposium of the CRC 51, Delmenhorst, Germany, October 24-26 (talk).
• Patzelt D, Wang H, Buchholz I, Rohde M, Gröbe L, Neumann A, Schulz S, Pradella S, Münch R, Jahn D Wagner-Döbler I, Tomasch J (2013). You are what you talk: Quorum sensing induces individualisation of the algal symbiont Dinoroseobacter shibae DFL-12. Annual Meeting of the German Society of General and Applied Microbiology (VAAM), Bremen, Germany, March 10-13 (poster).
• Petersen J (2013). Transposon Mutagenesis: Experimental distinction of the essential and the dispensable gene pool of Phaeobacter inhibens DSM17395. Retreat of the CRC 51, Wolfenbüttel, Germany, February 15^th (talk).
• Petersen J (2013). Plasmids: Extrachromosomal, extraordinary and essential: The mobilome of the Roseobacter clade. Retreat of the CRC 51, Wolfenbüttel, Germany, February 14^th (talk).
• Petersen J (2012). Transposon Mutagenesis – New project ideas. 7^th Status Seminar of the CRC 51, Delmenhorst, Germany, October 16^th (talk).
• Petersen J (2012). Plasmids – Project A5 Progress report and future perspectives. 7^th Status Seminar of the CRC 51, Delmenhorst, Germany, October 15^th (talk).
• Pradella S (2012). Dinoroseobacter shibae – Plasmide und Plasmid-Curing. Dinoroseobacter shibae seminar, TU Braunschweig, Germany, July 2^nd (talk).
• Frank O, Petersen J, Päuker O, Pradella S (2011). Genome sequence of Marinovum algicola - meet the marine mobilome. ProkaGENOMICS - 5^th European Conference on Prokaryotic and Fungal Genomics, Göttingen, Germany, September 18-21 (poster).
• Petersen J (2011). Think pink: photosynthesis, plasmids and the Roseobacter clade. 3^rd Status Seminar of the CRC 51, HZI, Braunschweig, Germany, September 15^th (talk).
• Buddruhs N, Frank O, Pradella S, Petersen J (2011). Brown becomes white – phenotypical changes of Phaeobacter gallaeciensis through the loss of its major plasmid. MIMAS (Microbial Interactions in Marine Systems) Symposium, Greifswald, Germany, August 6-8 (poster).
• Frank O, Petersen J, Päuker O, Pradella S (2011). Meet the marine mobilome: plasmid classification and the partitioned genome of Marinovum algicola. MIMAS (Microbial Interactions in Marine Systems) Symposium, Greifswald, Germany, August 6-8 (poster).
• Petersen J (2011). Think pink: roseobacters, plasmids and their classification in the genomics era. Julius Kühn Institute, Braunschweig, Germany, June 7^th (invited talk).
• Buddruhs N, Frank O, Michael V, Päuker O, Pradella S, Petersen J (2011). Comparative phenomics of the wild type Phaeobacter gallaeciensis and its 65 kb plasmid knock-out mutant. Annual Meeting of the German Society of General and Applied Microbiology (VAAM), Karlsruhe, Germany, April 3-6 (poster).
• Frank O, Buddruhs N, Michael V, Päuker O, Pradella S, Petersen J (2011). A novel approach for alphaproteobacterial plasmid classification. Annual Meeting of the German Society of General and Applied Microbiology (VAAM), Karlsruhe, Germany, April 3-6 (poster).
• Petersen J (2011). Compatibility and phylogeny – plasmid classification in the genomics era. Annual Meeting of the German Society of General and Applied Microbiology (VAAM), Karlsruhe, Germany, April 6^th (talk).
• Pradella S, Petersen J (2010). Evolution and significance of plasmids within the Roseobacter clade. 1^st Status Seminar of the CRC 51, Braunschweig, Germany, October 21^th (talk).
• Petersen J (2010). Dinoflagellates - The bizarre world of unicellular individualists, Biologische Anstalt Helgoland, Germany, September 20^th (talk).
• Petersen J (2010). The intriguing abundance of plasmids in the Roseobacter clade – a novel approach for their classification. Transregional Collaborative Research Center (CRC-51) Kick-off Symposium: Ecology, Physiology and Molecular Biology of the Roseobacter clade: Towards a Systems Biology Understanding of a Globally Important Clade of Marine Bacteria, HWK, Delmenhorst, Germany, June 14^th (talk).

Knowledge transfer

• Brinkmann H (2011). Guest scientist at the DSMZ, December 2011
• Brinkmann H (2013). Guest scientist at the DSMZ, January 2013
• Michael V (2011). Isolation and cultivation of fastidious dinoflagellates; guest technician hosted by C. Dungan and K. Reece, Virginia, USA, August 2011
• Ludewig A-K (2013). Exchange student hosted by H. Philippe and H. Brinkmann, Université de Montréal, Canada, May to June 2013

Excursions

• Petersen J, Frank O, Michael V (2013). Collection of macro-algae, Helgoland, Germany, June 4-6.
• Frank O (2011). Practical course in marine microbiology at the Biologische Anstalt Helgoland, Germany, September 2011.

Roseobacter plasmids in the media

• DSMZ Press Release (2016). „ Microorganisms Getting a Grip - Plasmids Control Marine Biofilm Formation”, Leibniz-Institute DSMZ, Braunschweig, Germany, March 11^th (DSMZ Press Release Roseobacter 2016).
• DSMZ Press Release (2015). „Cleverer Propellertausch bei Meeresbakterien - Flagellen bei Roseobacter über spezielle Plasmide vererbt“, Leibniz-Institute DSMZ, Braunschweig, Germany, June 22^th (DSMZ Press Release Roseobacter 2015).
• Laborjournal (2012). „Gen-Geflüster - Jörn Petersen fand bei pinken Meeresbakterien eine besondere Form der Kommunikation über Plasmide“, December 11^th (Laborjournal 2012).
• DRadio Wissen (2012). Interview with Jörn Petersen concerning our „Think Pink!“ publication (Petersen et al. 2012), broadcast July 17^th, news id=115268.
• DSMZ Press Release 8/12 (2012). „Think pink! Success of pink bacteria in oceans of the world”, Leibniz-Institute DSMZ, Braunschweig, Germany, July 16^th (DSMZ Press Release Roseobacter 2012).
• DSMZ Press Release (2010). „Rosa: die Trendfarbe für niedersächsische Forscher. Sonderforschungsbereich Roseobacter in Niedersachsen etabliert“, Leibniz-Institute DSMZ, Braunschweig, Germany, October 6^th (DSMZ Presse Realease Roseobater 2010).

Former Members

• Dr. Ann-Kathrin Ludewig-Klingner (*formerly Ann-Kathrin Ludewig)
• Dr. Stefanie Hahnke (*formerly Dr. Stefanie Müller)
• Oliver Frank
• Nora Buddruhs

Phylogenomics and functional genomics of the Roseobacter clade

Principal investigator(s): Markus Göker (formerly also Hans-Peter Klenk)
Postdocs: Dr. Jan P. Meier-Kolthoff
PhD students: Anne Fiebig, Palani Kannan Kandavel
Assistants: Carmen Scheuner, Marina García-Lopez
Student assistants: Lisa Weinhold, Ana Ilieva, Tugce Kaman

Objective

The main goal of this project is to improve our knowledge on the evolution of the Roseobacter clade with the aim to create a reliable genome-informed taxonomy that also considers the phenotypic features of clade members. For this purpose we conduct comparative, functional (phenotyping) and (phylo-)genomic studies. Separation of genealogy-defining information from non-phylogenetic signals in the genomic data allows us to use the latter for the investigation of correlations to ecological conditions and/or geographic origin of the members of the clade, with its ecologically diverse and geographically widespread organisms.

Methods and Results

We are currently genome-sequencing the majority of the Rhodobacteraceae type strains in the course of the KMG-2 project in conjunction with the Joint Genome Institute. These data are phylogenetically analysed using whole-genome bioinfomatic methods, similar to those to infer species boundaries from genome sequences. Phenotypic data are comprehensively collected from the literature to assist in taxonomic reclassifications and comparisons with the phylogeny. Selected genomic features are compared using phylogeny-aware methods with relevant ecological and phenotypic features such as the habitat. For instance, our recent study revealed the genomic adaptations of Rhodobacteraceae to marine environments. We also showed that the so-called "Roseobacter clade" might not be monophyletic and thus should rather not be called a clade. Since bacteriophages are of great interest in marine ecosystems in general and for Rhodobacteraceae in particular, we have developed the web service VICTOR for phage phylogeny and classification. Our earlier work within the SFB-TRR 51 yielded the R package opm for analysising phenotype microarray data.

Publications

Manuscripts in press

Bartling, P., Brinkmann, H., Bunk, B., Overmann, J., Göker, M., Petersen, J. The composite 259-kb plasmid of Martelella mediterranea DSM 17316T – A natural shuttle vector for horizontal gene transfer between Rhodobacteraceae and Rhizobiaceae. Frontiers in Microbiology, in press.

Publications 2014-2017

Breider, S., Scheuner, C., Schumann, P., Fiebig, A., Petersen, J., Pradella, S., Klenk, H.-P., Brinkhoff, T., Göker, M. Genome-scale data suggest reclassifications in the Leisingera-Phaeobacter cluster including proposals for Sedimentitalea gen. nov. and Pseudophaeobacter gen. nov. Frontiers in Microbiology 5: 416, 2014 (doi:10.3389/fmicb.2014.00416).

Breider, S., Teshima, H., Petersen, J., Fiebig, A., Chertkov, O., Dalingault, H., Chen, A., Pati, A., Goodwin, L.A., Chain, P., Detter, J.C., Ivanova, N.N., Lapidus, A., Rohde, M., Tindall, B.J., Kyrpides, N.C., Woyke, T., Simon, M., Göker, M., Klenk, H.-P., Brinkhoff, T. Complete genome sequence of Leisingera nanhaiensis strain DSM 24252^T isolated from marine sediment. Standards in Genomic Sciences 9: 687-703, 2014 (doi:10.4056/sigs.3828824).

Beyersmann PG, Tomasch J, Son K, Stocker R, Göker M, Wagner-Döbler I, Simon M, Brinkhoff T (2017) Dual function of tropodithietic acid as antibiotic and signaling molecule in global gene regulation of the probiotic bacterium Phaeobacter inhibens. Sci Rep 7: 730. 10.1038/s41598-017-00784-7 [doi];10.1038/s41598-017-00784-7 [pii].

Drüppel, K., Hensler, M., Trautwein, K., Koßmehl, S., Wöhlbrand, L., Schmidt-Hohagen, K., Ulbrich, M., Bergen, N., Meier-Kolthoff, J.P., Göker, M., Klenk, H.-P., Schomburg, D., Rabus, R.A. Pathways and substrate-specific regulation of amino acid degradation in Phaeobacter inhibens DSM 17395 (archetype of the marine Roseobacter clade). Environmental Microbiology 16: 218-138, 2014 (doi:10.1111/1462-2920.12276).

Frank, O., Pradella, S., Rohde, M., Scheuner, C., Klenk, H.-P., Göker, M., Petersen, J. Complete genome sequence of the Phaeobacter gallaeciensis type strain CIP 105210^T (= DSM 26640^T = BS107^T). Standards in Genomic Sciences 9: 914-932, 2014 (doi:10.4056/sigs.5179110).

Frank, O., Göker, M., Pradella, S., Petersen, J. Ocean's twelve: Flagellar and biofilm chromids in the multipartite genome of Marinovum algicola DG898 exemplify functional compartmentalization. Environmental Microbiology 17: 4019-4034, 2015 (doi:10.1111/1462-2920.12947).

Hofner, B., Boccuto, L., Göker, M. Controlling false discoveries in high-dimensional situations: Boosting with stability selection. BMC Bioinformatics 16: 144, 2015 (doi:10.1186/s12859-015-0575-3).

Kanukollu, S., Voget, S., Pohlner, M., Vandieken, V., Petersen, J., Kyrpides, N.C., Woyke, T., Shapiro, N., Göker, M., Klenk, H.-P., Cypionka, H., Engelen, B. Genome sequence of Shimia sp. SK013, a representative of the Roseobacter group isolated from marine sediment. Standards in Genomic Sciences 11: 25, 2016 (doi:10.1186/s40793-016-0143-0).

Lau, S.C.K., Riedel, T., Fiebig, A., Han, J., Huntemann, M., Petersen, J., Ivanova, N.N., Markowitz, V., Woyke, T., Göker, M., Kyrpides, N.C., Klenk, H.-P., Qian, P-Y. Genome sequence of the pink-pigmented marine bacterium Loktanella hongkongensis type strain (UST950701-009P^T), a representative of the Roseobacter group. Standards in Genomic Sciences 10: 51, 2015 (doi:10.1186/s40793-015-0050-9).

Meier-Kolthoff JP, Göker M. (2017) Genome-based phylogeny and classification of bacteriophages. Bioinformatics 2017: 1-9, 2017 (doi:10.1093/bioinformatics/btx440).

Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2014) Highly parallelized inference of large genome-based phylogenies. Concurrency and Computation: Practice and Experience 26: 1715-1729 (doi:10.1002/cpe.3112

Michael, V., Frank, O., Bartling, P., Scheuner, C., Göker, M., Brinkmann, H., Petersen, J. Biofilm-plasmids with a rhamnose operon are essential determinants of the “swim-or-stick” lifestyle in roseobacters. The ISME Journal 2016: 1-16, 2016 (doi:10.1038/ismej.2016.30).

Riedel, T., Spring, S., Fiebig, A., Scheuner, C., Petersen, J., Göker, M., Klenk, H.-P. Genome sequence of the Roseovarius mucosus type strain (DSM 17069^T), a bacteriochlorophyll a-containing representative of the marine Roseobacter group isolated from the dinoflagellate Alexandrium ostenfeldii. Standards in Genomic Sciences 10: 17, 2015 (doi:10.1186/1944-3277-10-17).

Riedel, T., Fiebig, A., Göker, M., Klenk, H.-P. Complete genome sequence of the bacteriochlorophyll a-containing Roseibacterium elongatum type strain (DSM 19469^T), a representative of the Roseobacter clade isolated from Australian coast sand. Standards in Genomic Sciences 9: 840-854, 2014 (doi:10.4056/sigs.5541028).

Riedel, T., Fiebig, A., Han, J., Huntemann, M., Spring, S., Petersen, J., Ivanova, N.N., Markowitz, V., Woyke, T., Göker, M., Kyrpides, N.C., Klenk, H.-P. Genome sequence of the Wenxinia marina type strain (DSM 24838^T), a representative of the Roseobacter clade isolated from oilfield sediments. Standards in Genomic Sciences 9: 855-865, 2014 (doi:10.4056/sigs.5601028).

Riedel, T., Spring, S., Fiebig, A., Petersen, J., Göker, M., Klenk, H.-P. Genome sequence of the pink to light reddish-pigmented Rubellimicrobium mesophilum type strain (DSM 19309^T), a representative of the Roseobacter clade isolated from soil, and emended description of the species. Standards in Genomic Sciences 9: 902-913, 2014 (doi:10.4056/sigs.5621012).

Riedel, T., Spring, S., Fiebig, A., Petersen, J., Kyrpides, N.C., Göker, M., Klenk, H.-P. Genome sequence of the exopolysaccharide-producing Salipiger mucosus type strain (A3^T), a moderately halophilic member of the Roseobacter clade. Standards in Genomic Sciences 9: 1331-1343, 2014 (doi:10.4056/sigs.4909790).

Simon, M., Scheuner, C., Meier-Kolthoff, J.P., Brinkhoff, T., Wagner-Döbler, I., Ulbrich, M., Klenk, H.-P., Schomburg, D., Petersen, J., Göker, M. Phylogenomics of Rhodobacteraceae reveals evolutionary adaptation to marine and non-marine habitats. The ISME Journal 2017, 1-17, 2017 (doi:10.1038/ismej.2016.198).

Voget, S., Göker, M., Brinkhoff, T. Genomik: Grundlage zum Verständnis des Erfolgs der Roseobacter-Gruppe. BIOSpektrum 20: 279-282, 2014.

Publications 2011-2013

Beyersmann, P.G., Chertkov, O., Petersen, J., Fiebig, A., Chen, A., Pati, A., Ivanova, N.N., Lapidus, A., Goodwin, L.A., Chain, P., Detter, J.C., Rohde, M., Gronow, S., Kyrpides, N.C., Woyke, T., Simon, M., Göker, M., Klenk, H.-P., Brinkhoff, T. Genome sequence of Phaeobacter caeruleus type strain (DSM 24564^T), a surface-associated member of the marine Roseobacter clade. Standards in Genomic Sciences 8: 403-419, 2013 (doi:10.4056/sigs.3927623).

Breider S, Teshima H, Petersen J, Fiebig A, 12 co-authors, Simon M, Göker M, Klenk HP, Brinkhoff T (2013) Complete genome sequence of Leisingera nanhaiensis strain DSM 24252^T isolated from marine sediment. Stand Genomic Sci, 9: 687-703.

Buddruhs, N., Chertkov, O., Petersen, J., Fiebig, A., Chen, A., Pati, A., Ivanova, N.N., Lapidus, A., Goodwin, L.A., Chain, P., Detter, J.C., Gronow, S., Kyrpides, N.C., Woyke, T., Göker, M., Brinkhoff, T., Klenk, H.-P. Complete genome sequence of the marine methyl-halide oxidizing Leisingera methylohalidivorans type strain (DSM 14336^T), a member of the Roseobacter clade. Standards in Genomic Sciences 9: 128-141, 2013 (doi:10.4056/sigs.4297965).

Buddruhs, N., Pradella, S., Göker, M., Päuker, O., Michael, V., Pukall, R., Spröer, C., Schumann, P., Petersen, J., Brinkhoff, T. Molecular and phenotypic analyses reveal the non-identity of the Phaeobacter gallaeciensis type strain deposits CIP 105210^T and DSM 17395. International Journal of Systematic and Evolutionary Microbiology 63: 4340-4349, 2013 (doi:10.1099/ijs.0.053900-0).

Dogs, M., Teshima, H., Petersen, J., Fiebig, A., Chertkov, O., Dalingault, H., Chen, A., Pati, A., Goodwin, L.A., Chain, P., Detter, J.C., Ivanova, N.N., Lapidus, A., Rohde, M., Gronow, S., Kyrpides, N.C., Woyke, T., Simon, M., Klenk, H.-P., Göker, M., Brinkhoff, T. Genome sequence of Phaeobacter daeponensis type strain (DSM 23529^T), a facultatively anaerobic bacterium isolated from marine sediment, and emendation of Phaeobacter daeponensis. Standards in Genomic Sciences 9: 142-159, 2013 (doi:10.4056/sigs.4287962).

Dogs, M., Voget, S., Teshima, H., Petersen, J., Fiebig, A., Davenport, K.W., Dalingault, H., Chen, A., Pati, A., Ivanova, N.N., Goodwin, L.A., Chain, P., Detter, J.C., Rohde, M., Gronow, S., Kyrpides, N.C., Woyke, T., Simon, M., Klenk, H.-P., Göker, M., Brinkhoff, T. Genome sequence of Phaeobacter inhibens type strain (T5^T), a secondary-metabolite producing member of the marine Roseobacter clade, and emendation of the species Phaeobacter inhibens. Standards in Genomic Sciences 9: 334-350, 2013 (doi:10.4056/sigs.4448212).

Drüppel K, Hensler M, Trautwein K, Koßmehl S, Wöhlbrand L, Schmidt-Hohagen K, Ulbrich M, Bergen N, Meier-Kolthoff J, Göker M, Klenk HP, Schomburg D, Rabus, AR (2013) Pathways and substrate-specific regulation of amino acid degradation in Phaeobacter inhibens DSM 17395 (archetype of the marine Roseobacter clade). Environ Microbiol, submitted.

Fiebig, A., Pradella, S., Petersen, J., Michael, V., Päuker, O., Rohde, M., Göker, M., Klenk, H.-P., Wagner-Döbler, I. Genome of the marine alphaproteobacterium Hoeflea phototrophica type strain (DFL-43^T). Standards in Genomic Sciences 7: 440-444, 2013 (doi:10.4056/sigs.3486982).

Fiebig, A., Pradella, S., Petersen, J., Päuker, O., Michael, V., Lünsdorf, H., Göker, M., Klenk, H.-P., Wagner-Döbler, I. Genome of the R-body producing marine alphaproteobacterium Labrenzia alexandrii type strain (DFL-11^T). Standards in Genomic Sciences 7: 413-426, 2013 (doi:10.4056/sigs.3456959).

Fiebig, A., Riedel, T., Gronow, S., Klenk, H.-P., Göker, M. Genome sequence of the reddish-pigmented Rubellimicrobium thermophilum type strain (DSM 16684^T), a member of the Roseobacter clade. Standards in Genomic Sciences 8: 480-490, 2013 (doi:10.4056/sigs.4247911).

Freese, H., Dalingault, H., Petersen, J., Pradella, S., Fiebig, A., Davenport, K.W., Teshima, H., Chen, A., Pati, A., Ivanova, N.N., Goodwin, L.A., Chain, P., Detter, J.C., Rohde, M., Gronow, S., Kyrpides, N.C., Woyke, T., Brinkhoff, T., Göker, M., Overmann, J., Klenk, H.-P. Genome sequence of the phage-gene rich marine Phaeobacter arcticus type strain DSM 23566^T. Standards in Genomic Sciences 8: 450-464, 2013 (doi:10.4056/sigs.383362).

Göker, M., Klenk, H.-P. Phylogeny-driven target selection for genome-sequencing (and other) projects. Standards in Genomic Sciences 8: 360-374, 2013 (doi:10.4056/sigs.3446951).

Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14: 60.

Petersen, J., Frank, O., Göker, M., Pradella, S. Extrachromosomal, Extraordinary and Essential – The Plasmids of the Roseobacter Clade. Applied Microbiology and Biotechnology 97: 2805-2815, 2013.

Riedel, T., Fiebig, A., Petersen, J., Gronow, S., Göker, M., Klenk, H.-P. Genome sequence of the Litoreibacter arenae type strain (DSM 19593^T), a member of the Roseobacter clade isolated from sea sand. Standards in Genomic Sciences 9: 117-127, 2013 (doi:10.4056/sigs.4258318).

Riedel, T., Teshima, H., Petersen, J., Fiebig, A., Davenport, K.W., Dalingault, H., Erkkila, T., Gu, W., Munk, A.C., Xu, Y., Chen, A., Pati, A., Ivanova, N.N., Goodwin, L.A., Chain, P., Detter, J.C., Rohde, M., Gronow, S., Kyrpides, N.C., Woyke, T., Göker, M., Brinkhoff, T., Klenk, H.-P. Genome sequence of the Leisingera aquimarina type strain (DSM 24565^T), a member of the marine Roseobacter clade rich in extrachromosomal elements. Standards in Genomic Sciences 8: 389-402, 2013 (doi:10.4056/sigs.3858183).

Sikorski, J., Göker, M., Vaas, L.A.I. Analyse von Hochdurchsatzdaten – Struktur und Umfang eines neu entwickelten Software-Pakets. GIT Labor-Fachzeitschrift 56: 528-530, 2012.

Vaas, L.A.I., Sikorski, J., Hofner, B., Buddruhs, N., Fiebig, A., Klenk, H.-P., Göker, M. opm: An R package for analysing OmniLog® Phenotype MicroArray Data. Bioinformatics 29: 1823-1824, 2013 (doi:10.1093/bioinformatics/btt291).

Vaas, L.A.I., Sikorski, J., Michael, V., Göker, M., Klenk, H.-P. Visualization and curve-parameter estimation strategies for efficient exploration of Phenotype Microarray kinetics. PLoS ONE 7: e34846, 2012 (doi:10.1371/journal.pone.0034846).

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Population structure and divergence in the Roseobacter clade – implications for the ecology and evolution

Principal investigator: Prof. Dr. Jörg Overmann
Scientist: Dr. Heike M. Freese

Aim

Bacteria of the Roseobacter clade represent an abundant but also phylogenetically and physiologically diverse group of marine bacteria. The evolutionary mechanisms underlying this high diversity (such as selective forces) have remained so far unknown. Therefore, we will identify the intraspecific population structure of the model organisms Phaeobacter inhibens and P. gallaeciensis in order to identify the specific evolutionary forces that are responsible for diversification of this important bacterial group.

A collection of 88 available Phaeobacter inhibens and P. gallaeciensis strains is investigated. The 16S rRNA genes of these strains show a close similarity of 99.5%. Comparisons of the complete internal transcribed spacer sequences and MALDI-TOF profiles showed that the strains fall in distinct subgroups. For a comprehensive analysis of the population structure of Phaeobacter inhibens and P. gallaeciensis, the genomes of representative strains were sequenced and are currently being analyzed.

In parallel, high-throughput isolation strategies are applied to enrich additional Phaeobacter-strains from the environment. Phaeobacter-related bacteria were successfully enriched. Variations in the phylogenetic composition among the different habitats suggest a habitat preference of the different lineages of the Roseobacter clade.

Methods

The Phaeobacterstrains are grown in appropriate media (Fig. 1) and their DNA extracted. For genome-sequencing, Illumina and PacBio-technology are employed. The two sequence types are separately assembled de novo and the created contigs are co-assembled afterwards. Then, the population structure is analysed (e.g. by split decomposition-analysis) and population genetics parameters (such as recombination rate : mutation rate r/n, effective population size, dN/dS) are determined from genes and genomes. Results will be compared with habitat parameters but also with the phenotypic characteristics of the strains.

Fig. 1.

In order to isolate Phaeobacter sp. from the environment, samples were taken at the North Sea coast in Neuharlingersiel (Fig. 2) and also during cruises of RV Sonne to the Pacific Ocean. Liquid and biofilm-specific high-throughput cultivation are performed using defined media. Success of cultivation is checked via specific screening PCR and sequencing.

Fig. 2.

Expeditions

Expedition SO254 (RV Sonne, February 2017, Southwest Pacific, Auckland (New Zealand) - Auckland): Functional diversity of bacterial communities and the metabolome in the water column, sediment and in sponges in the southwest Pacific around New Zealand – Population structure and divergence in the Roseobacter group

Expedition SO248 (RV Sonne, May 2016, Pacific transect, Auckland (New Zealand) - Dutch Harbour (Alaska)): Functional diversity of bacterial communities and the geometabolome in the central and north Pacific – Population structure and divergence in the Roseobacter group

Publications

Crenn K, Serpin D, Lepleux C, Spröer C, Bunk B, Overmann J, Jeanthon C (2016) Silicimonas algicola gen. nov., sp. nov., a novel member of the Roseobacter clade isolated from the cell surface of the marine diatom Thalassiosira delicatula. Int. J. Syst. Evol. Microbiol. 66: 4580-4588.

Breider S, Freese HM, Spröer C, Simon M, Overmann J, Brinkhoff T (2017) Phaeobacter porticola sp. nov., an antibiotic producing bacterium isolated from a harbor in the southern North Sea. Int J Syst Evol Microbiol. 67: 2153-2159.

Freese HM, Methner A, Overmann J (2017) Adaptation of biofilm bacteria to the open ocean: A genomically distinct subpopulation of Phaeobacter gallaeciensis colonizes Pacific mesozooplankton. Front Microbiol 8: 1659.

Overmann J, Lepleux C (2016) Marine Bacteria and Archaea: Diversity, Adaptations, and Culturability. In: Stal LJ, and Cretoiu MS (eds.) The Marine Microbiome. Chapter 2. Springer International Publishing, Switzerland. p. 21- 55.

Shang Y, Sikorski J, Bonkowski M, Fiore-Donno A-M, Kandeler E, Boeddinghaus R, Marhan S, Solly E, Schrumpf M, Schöning I, Tesfaye W, Buscot F, Overmann J (2017) Inferring interactions in complex microbial communities from nucleotide sequence data and environmental parameters. PLoS One 12: e0173765. https://doi.org/10.1371/journal.pone.0173765

Sonnenschein EC, Broughton C, Phippen W, Nielsen KF, Mateiu RV, Melchiorsen J, Gram L, Overmann J, Freese HM (2017) Phaeobacter piscinae sp. nov., a novel species of the roseobacter group and potential aquaculture probiont. Int J Syst Evol Microbiol. In press.

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Linking the exometabolome of selected pelagic organisms of the Roseobacter clade to marine dissolved organic matter

Principal investigators: Prof. Dr. Thorsten Dittmar, Dr. Jutta Niggemann, Prof. Dr. Meinhard Simon

Post docs:

PhD students:

Project outline:

Scientific questions

Marine dissolved organic matter (DOM) plays a vital role for life on Earth. It links organic matter production and decay in the water column because algal products can only be taken up by prokaryotic consumers as small dissolved molecules. Most of DOM is turned over by heterotrophic prokaryotes within hours and days after production. A small fraction of DOM, however, resists prokaryotic degradation. This refractory fraction of DOM has persisted in the ocean for thousands of years, and has accumulated to the largest pool of organic carbon in the ocean, approx. 30 times larger than the pool of particulate organic carbon. DOM remains arguably the most mysterious carbon pool on earth. It is an enigma how reduced organic molecules persist for millennia in an oxygen- and nutrient-rich environment in the deep ocean. Heterotrophic prokaryotes can acquire chemical energy and essential elements, such as nitrogen and phosphorous, from the oxidation of DOM, and most of the DOM is small enough in molecular size to be directly taken up by heterotrophic prokaryotes. In this project we aim at a better understanding of DOM in two aspects: 1 - The reasons behind millennium-scale stability of DOM, and 2 - Molecular interactions between prokaryotes and DOM in marine systems. The well characterized Roseobacter clade provides us with the unique opportunity to test hypotheses under well-constrained settings in the laboratory and in the field.

The advent of ultrahigh-resolution mass spectrometry via the Fourier transform ion cyclotron resonance technique (FT-ICR MS) has allowed unprecedented insights into the molecular composition of marine DOM. Over the past few years we identified >10,000 molecular formulae of compounds in DOM. The structural isomers behind these formulae are unknown, but in a recent study we estimated that there are more than 10¹⁵ different molecules in each liter of seawater. The concentration of individual compounds is so low that molecular diffusion limits uptake by microorganisms which is probably the main reason for the persistence of DOM in the ocean.

We hypothesize that part of the enormous molecular diversity in DOM is already present in the exometabolome of a single species. The expression of different metabolic pathways due to different growth or substrate conditions further increases the molecular diversity. In addition, each bacterial species has a specific molecular fingerprint. The interplay of species further increases the complexity of the exometabolome. This is also true for members of the Roseobacter clade and, therefore, relevant members of pelagic subclusters of this clade are involved in shaping the exometabolome of a given situation in pelagic ecosystems.

Aims, work program and methods

In order to understand the specific role and function of relevant members of pelagic subclusters of the Roseobacter clade (RCA, CHABI-5, NAC11-6, SH6-1, Octadecabacter) for shaping the marine exometabolome we will carry out growth experiments with model organisms of these subclusters and examine their exometabolome at typical situations of their growth cycle, initial conditions, mid-exponential growth phase, early and late stationary phase. The model organisms will be grown on defined single carbon sources, on algal exudates, at varying growth conditions (dark, light-dark, enhanced CO partial pressure, different temperatures). Further, selected experiments will be done with mixed cultures with one organism of the Roseobacter clade, utilizing preferentially low molecular weight compounds, and one Flavobacterium, rich in hydrolytic enzyme activities and thus capable of breaking down biopolymers, in order to examine the impact of bacterial interactions on the exometabolome.

We will molecularly characterize the exometabolome through a most comprehensive and holistic analytical approach via FT-ICR-MS. This approach will provide us with the molecular formulae of most compounds present in the exometabolome of our experiments. These molecular fingerprints can be compared to our extensive in-house data bank of the DOM geometabolome of >1000 seawater samples from around the globe. In collaboration within this CRC, a selected number of samples will be molecularly characterized by more conventional metabolic analyses. The analytical window of these techniques is more narrow compared to FT-ICR-MS, but quantitative and structural information can be obtained which will be highly complementary to FT-ICR-MS. Growth of the bacteria will be monitored by flow cytometry. Further, the physiological activity of the bacteria will be studied by hydrolytic enzyme activities (leucine aminopeptidase, a- and b-glucosidase, chitinase), transcriptomic and in selected experiments also proteomic profiling of the four selected growth stages.

Publications

Osterholz H, Niggemann J, Giebel H-A, Simon M, Dittmar T (2015) Inefficient microbial production of refractory dissolved organic matter in the ocean. Nature Commun 6: 7422.

Lucas J, Koester I, Wichels A, Niggemann J, Dittmar T, Callies U, Wiltshire KH, Gerdts G (2016) Short-term dynamics of North Sea bacterioplankton-dissolved organic matter coherence on molecular level. Front Microbiol 7: 321.

Moran MA, Kujawinski EB, Stubbins A, Fatland R, Aluwihare LI, Buchan A, Crump BC, Dorrestein PC, Dyhrman ST, Hess NJ, Howe B, Longnecker K, Medeiros PM, Niggemann J, Obernosterer I, Repeta DJ, Waldbauer JR (2016) Deciphering ocean carbon in a changing world. PNAS 113: 3143-3151.

Osterholz H, Singer G, Wemheuer B, Daniel R, Simon M, Niggemann J, Dittmar T (2016) Deciphering associations between dissolved organic molecules and bacterial communities in a pelagic marine system. ISME J 7: 1717-1730.

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