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Biogeography and environmental genomics of the Roseobacter-affiliated pelagic CHAB-I-5 lineage

Nature Microbiology volume 1, Article number: 16063 (2016) Cite this article

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Abstract

The identification and functional characterization of microbial communities remains a prevailing topic in microbial oceanography as information on environmentally relevant pelagic prokaryotes is still limited. The Roseobacter group, an abundant lineage of marine Alphaproteobacteria, can constitute large proportions of the bacterioplankton. Roseobacters also occur associated with eukaryotic organisms and possess streamlined as well as larger genomes from 2.2 to >5 Mpb. Here, we show that one pelagic cluster of this group, CHAB-I-5, occurs globally from tropical to polar regions and accounts for up to 22% of the active North Sea bacterioplankton in the summer. The first sequenced genome of a CHAB-I-5 organism comprises 3.6 Mbp and exhibits features of an oligotrophic lifestyle. In a metatranscriptome of North Sea surface waters, 98% of the encoded genes were present, and genes encoding various ABC transporters, glutamate synthase and CO oxidation were particularly upregulated. Phylogenetic gene content analyses of 41 genomes of the Roseobacter group revealed a unique cluster of pelagic organisms distinct from other lineages of this group, highlighting the adaptation to life in nutrient-depleted environments.

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Figure 1: Global distribution of the CHAB-I-5 cluster based on the detection of SSU rRNA genes by cluster-specific PCR and on mapping the origin of sequences from public databases.
Figure 2: Bacterial abundance, chlorophyll a concentrations and relative abundance of the CHAB-I-5 cluster.
Figure 3: Phylogenomic trees of 41 sequenced Roseobacter group genomes.
Figure 4: Circular plot of the genomes of six members of the PRC in comparison to the genome of CHAB-I-5 strain SB2.
Figure 5: Expression patterns of selected genes and gene clusters of strain SB2 and Planktomarina temperata RCA23 at station 13 in the North Sea.

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References

  1. Amin, S. A. et al. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 552, 98–101 (2015).

    Article  Google Scholar 

  2. Buchan, A., González, J. M. & Moran, M. A. Overview of the marine Roseobacter lineage. Appl. Environ. Microbiol. 71, 5665–5677 (2005).

    Article  Google Scholar 

  3. Buchan, A., LeCleir, G. R., Gulvik, C. A. & González, J. M. Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nature Rev. Microbiol. 12, 686–698 (2014).

    Article  Google Scholar 

  4. Giovannoni, S. J. & Stingl, U. Molecular diversity and ecology of microbial plankton. Nature 437, 343–348 (2005).

    Article  Google Scholar 

  5. Pommier, T., Pinhassi, J. & Hagström, Å. Biogeographic analysis of ribosomal RNA clusters from marine bacterioplankton. Aquat. Microb. Ecol. 41, 79–89 (2005).

    Article  Google Scholar 

  6. Selje, N., Simon, M. & Brinkhoff, T. A newly discovered Roseobacter cluster in temperate and polar oceans. Nature 427, 445–448 (2004).

    Article  Google Scholar 

  7. Yooseph, S. et al. Genomic and functional adaptation in surface ocean planktonic prokaryotes. Nature 468, 60–66 (2010).

    Article  Google Scholar 

  8. Cunliffe, M. Correlating carbon monoxide oxidation with cox genes in the abundant marine Roseobacter clade. ISME J. 5, 685–691 (2011).

    Article  Google Scholar 

  9. Wagner-Döbler, I. et al. The complete genome sequence of the algal symbiont Dinoroseobacter shibae: a hitchhiker's guide to life in the sea. ISME J. 4, 61–77 (2010).

    Article  Google Scholar 

  10. Moran, M. A., Reisch, C. R., Kiene, R. P. & Whitman, W. B. Genomic insights into bacterial DMSP transformations. Annu. Rev. Mar. Sci. 4, 523–542 (2012).

    Article  Google Scholar 

  11. Thole, S. et al. Phaeobacter gallaeciensis genomes from globally opposite locations reveal high similarity of adaptation to surface life. ISME J. 6, 2229–2244 (2012).

    Article  Google Scholar 

  12. Luo, H., Löytynoja, A. & Moran, M. A. Genome content of uncultivated marine roseobacters in the surface ocean. Environ. Microbiol. 14, 41–51 (2012).

    Article  Google Scholar 

  13. West, N. J., Obernosterer, I., Zemb, O. & Lebaron, P. Major differences of bacterial diversity and activity inside and outside of a natural iron-fertilized phytoplankton bloom in the Southern Ocean. Environ. Microbiol. 10, 738–756 (2008).

    Article  Google Scholar 

  14. Giebel, H. A., Brinkhoff, T., Zwisler, W., Selje, N. & Simon, M. Distribution of Roseobacter RCA and SAR11 lineages and distinct bacterial communities from the subtropics to the Southern Ocean. Environ. Microbiol. 11, 2164–2178 (2009).

    Article  Google Scholar 

  15. Giebel, H.-A. et al. Distribution of Roseobacter RCA and SAR11 lineages in the North Sea and characteristics of an abundant RCA isolate. ISME J. 5, 8–19 (2011).

    Article  Google Scholar 

  16. Giebel, H. A. et al. 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 (2013).

    Article  Google Scholar 

  17. Voget, S. et al. Adaptation of an abundant Roseobacter RCA organism to pelagic systems revealed by genomic and transcriptomic analyses. ISME J. 9, 371–384 (2015).

    Article  Google Scholar 

  18. González, J. M. et al. Bacterial community structure associated with a dimethylsulfoniopropionate-producing North Atlantic algal bloom. Appl. Environ. Microbiol. 66, 4237–4246 (2000).

    Article  Google Scholar 

  19. Landa, M., Blain, S., Christaki, U., Monchy, S. & Obernosterer, I. Shifts in bacterial community composition associated with increased carbon cycling in a mosaic of phytoplankton blooms. ISME J. 10, 39–50 (2016). .

    Article  Google Scholar 

  20. Varaljay, V. A. et al. Single-taxon field measurements of bacterial gene regulation controlling DMSP fate. ISME J. 9, 1677–1686 (2015).

    Article  Google Scholar 

  21. Schäfer, H., Servais, P. & Muyzer, G. Successional changes in the genetic diversity of a marine bacterial assemblage during confinement. Arch. Microbiol. 173, 138–145 (2000).

    Article  Google Scholar 

  22. Lekunberri, I. et al. The phylogenetic and ecological context of cultured and whole genome-sequenced planktonic bacteria from the coastal NW Mediterranean Sea. Syst. Appl. Microbiol. 37, 216–228 (2014).

    Article  Google Scholar 

  23. Yang, S. J., Kang, I. & Cho, J. C. Expansion of cultured bacterial diversity by large-scale dilution-to-extinction culturing from a single seawater sample. Microb. Ecol. 71, 29–43 (2016).

    Article  Google Scholar 

  24. Henriques, I. S., Almeida, A., Cunha, Â. & Correia, A. Molecular sequence analysis of prokaryotic diversity in the middle and outer sections of the Portuguese estuary Ria de Aveiro. FEMS Microbiol. Ecol. 49, 269–279 (2004).

    Article  Google Scholar 

  25. Buchan, A., Hadden, M. & Suzuki, M. T. Development and application of quantitative-PCR tools for subgroups of the Roseobacter clade. Appl. Environ. Microbiol. 75, 7542–7547 (2009).

    Article  Google Scholar 

  26. Rich, V. I., Pham, V. D., Eppley, J., Shi, Y. & DeLong, E. F. Time-series analyses of Monterey Bay coastal microbial picoplankton using a ‘genome proxy’ microarray. Environ. Microbiol. 13, 116–134 (2011).

    Article  Google Scholar 

  27. Hahnke, S. et al. Physiological diversity of Roseobacter clade bacteria co-occurring during a phytoplankton bloom in the North Sea. Syst. Appl. Microbiol. 36, 39–48 (2013).

    Article  Google Scholar 

  28. Suzuki, M. T. et al. Phylogenetic screening of ribosomal RNA gene-containing clones in Bacterial Artificial Chromosome (BAC) libraries from different depths in Monterey Bay. Microb. Ecol. 48, 473–488 (2004).

    Article  Google Scholar 

  29. Alonso-Gutiérrez, J. et al. Bacterioplankton composition of the coastal upwelling system of ‘Ría de Vigo’, NW Spain. FEMS Microbiol. Ecol. 70, 493–505 (2009).

    Article  Google Scholar 

  30. Wemheuer, B. et al. 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 (2014).

    Article  Google Scholar 

  31. Luo, H., Swan, B. K., Stepanauskas, R., Hughes, A. L. & Moran, M. A. Evolutionary analysis of a streamlined lineage of surface ocean roseobacters. ISME J. 8, 1428–1439 (2014).

    Article  Google Scholar 

  32. Newton, R. J. et al. Genome characteristics of a generalist marine bacterial lineage. ISME J. 4, 784–798 (2010).

    Article  Google Scholar 

  33. Durham, B. P. et al. Draft genome sequence of marine alphaproteobacterial strain HIMB11, the first cultivated representative of a unique lineage within the Roseobacter clade possessing an unusually small genome. Stand Genomic Sci. 9, 632–645 (2014).

    Article  Google Scholar 

  34. Tripp, H. J. et al. SAR11 marine bacteria require exogenous reduced sulphur for growth. Nature 452, 741–744 (2008).

    Article  Google Scholar 

  35. Klingner, A. et al. 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, 2408–2422 (2015).

    Article  Google Scholar 

  36. Kolowith, L. C., Ingall, E. D. & Benner, R. Composition and cycling of marine organic phosphorus. Limnol. Oceanogr. 46, 309–320 (2001).

    Article  Google Scholar 

  37. Sowell, S. M. et al. Transport functions dominate the SAR11 metaproteome at low-nutrient extremes in the Sargasso Sea. ISME J. 3, 93–105 (2009).

    Article  Google Scholar 

  38. Feingersch, R. et al. Potential for phosphite and phosphonate utilization by Prochlorococcus. ISME J. 6, 827–834 (2012).

    Article  Google Scholar 

  39. Giovannoni, S. J. et al. Genome streamlining in a cosmopolitan oceanic bacterium. Science 309, 1242–1245 (2005).

    Article  Google Scholar 

  40. Lauro, F. M. et al. The genomic basis of trophic strategy in marine bacteria. Proc. Natl Acad. Sci. USA 106, 15527–15533 (2009).

    Article  Google Scholar 

  41. Wemheuer, B. et al. 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 (2015).

    Article  Google Scholar 

  42. Ghiglione, J.-F. et al. Pole-to-pole biogeography of surface and deep marine bacterial communities. Proc. Natl Acad. Sci. USA 109, 17633–17638 (2012).

    Article  Google Scholar 

  43. Brown, M. V., Ostrowski, M., Grzymski, J. J. & Lauro, F. M. A trait based perspective on the biogeography of common and abundant marine bacterioplankton clades. Mar. Genom. 15, 17–28 (2014).

    Article  Google Scholar 

  44. Luo, H., Csuros, M., Hughes, A. L. & Moran, M. A. Evolution of divergent life history strategies in marine alphaproteobacteria. MBio 4, e00373–13 (2013).

    Article  Google Scholar 

  45. Osterholz, H. et al. Deciphering associations between dissolved organic molecules and bacterial communities in a pelagic marine system. ISME J. doi:10.1038/ismej.2015.231 (2016).

    Article  CAS  PubMed  Google Scholar 

  46. Baldwin, A. J. et al. Microbial diversity in a Pacific Ocean transect from the Arctic to Antarctic circles. Aquat. Microb. Ecol. 41, 91–102 (2005).

    Article  Google Scholar 

  47. Gram, L., Melchiorsen, J. & Bruhn, J. B. Antibacterial activity of marine culturable bacteria collected from a global sampling of ocean surface waters and surface swabs of marine organisms. Mar. Biotechnol. 12, 439–451 (2010).

    Article  Google Scholar 

  48. Wietz, M. et al. Wide distribution of closely related, antibiotic-producing Arthrobacter strains throughout the Arctic Ocean. Appl. Environ. Microbiol. 78, 2039–2042 (2012).

    Article  Google Scholar 

  49. Zhou, J., Bruns, M. A. & Tiedje, J. M. DNA recovery from soils of diverse composition. Appl. Environ. Microbiol. 62, 316–322 (1996).

    Google Scholar 

  50. Ludwig, W. et al. ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363–1371 (2004).

    Article  Google Scholar 

  51. Angly, F. E. et al. CopyRighter: a rapid tool for improving the accuracy of microbial community profiles through lineage-specific gene copy number correction. Microbiome 2, 11 (2014).

    Article  Google Scholar 

  52. Ashelford, K. E., Chuzhanova, N. A., Fry, J. C., Jones, A. J. & Weightman, A. J. At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl. Environ. Microbiol. 71, 7724–7736 (2005).

    Article  Google Scholar 

  53. Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7, 335–336 (2010).

    Article  Google Scholar 

  54. Hahnke, S. et al. Planktotalea frisia gen. nov., sp. nov., isolated from the southern North Sea. Int. J. Syst. Evol. Microbiol. 62, 1619–1624 (2012).

    Article  Google Scholar 

  55. Zech, H. et al. Growth phase-dependent global protein and metabolite profiles of Phaeobacter gallaeciensis strain DSM 17395, a member of the marine Roseobacter-clade. Proteomics 9, 3677–3697 (2009).

    Article  Google Scholar 

  56. Martens, T. et al. Reclassification of Roseobacter gallaeciensis Ruiz-Ponte et al. 1998 as Phaeobacter gallaeciensis gen. nov., comb. nov., description of Phaeobacter inhibens sp. nov., reclassification of Ruegeria algicola (Lafay et al. 1995) Uchino et al. 1999 as Marinovum algicola gen. nov., comb. nov., and emended descriptions of the genera Roseobacter, Ruegeria and Leisingera. Int. J. Syst. Evol. Microbiol. 56, 1293–1304 (2006).

    Article  Google Scholar 

  57. Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comp. Biol. 19, 455–477 (2012).

    Article  Google Scholar 

  58. Seemann, T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069 (2014).

    Article  Google Scholar 

  59. Markowitz, V. M. et al. IMG 4 version of the integrated microbial genomes comparative analysis system. Nucleic Acids Res. 42, D560–D567 (2014).

    Article  Google Scholar 

  60. Lechner, M. et al. Proteinortho: detection of (co-)orthologs in large-scale analysis. BMC Bioinformatics 12, 124 (2011).

    Article  Google Scholar 

  61. Edgar, R. C. & Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).

    Article  Google Scholar 

  62. Castresana, J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540–552 (2000).

    Article  Google Scholar 

  63. Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).

    Article  Google Scholar 

  64. Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L. & Wold, B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods 5, 621–628 (2008).

    Article  Google Scholar 

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Acknowledgements

The authors thank J. Orchard, A. Neumann and O. Thomsen for their help in the laboratory, J. Lucas for the water sample from Helgoland and the crews of RV Heincke (grant no. AWI-HE361_00) and RV Polarstern (grant nos. AWI-PS ANT28-2_00, AWI-PS ANT28-4_00 and AWI-PS ANT28-5_00) for their support on board ship. The EAGER 2011 cruise was organized by the Continental Shelf Project of the Kingdom of Denmark and the Galathea 3 expedition was under the auspices of the Danish Expedition Foundation. This work was supported by the Deutsche Forschungsgemeinschaft (DFG) within the Transregional Collaborative Research Centre ‘Roseobacter’ (TRR 51).

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Authors and Affiliations

  1. Institute for Chemistry and Biology of the Marine Environment, University of Oldenburg, Oldenburg D-26111, Germany

    Sara Billerbeck, Helge-Ansgar Giebel, Thorsten Brinkhoff & Meinhard Simon

  2. Genomic and Applied Microbiology & Göttingen Genomics Laboratory, Institute of Microbiology and Genetics, University of Göttingen, Göttingen D-37077, Germany

    Bernd Wemheuer, Sonja Voget, Anja Poehlein & Rolf Daniel

  3. Department of Systems Biology, Technical University of Denmark, Lyngby DK-2800 Kgs, Denmark

    Lone Gram

  4. Center for Environmental Diagnostics and Bioremediation, University of West Florida, Pensacola, 32514, Florida, USA

    Wade H. Jeffrey

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Contributions

S.B., T.B. and M.S. designed the study. S.B. carried out the analyses of the phylogenetic cluster, biogeography and qPCR, and isolation of strain SB2. H.A.G. participated in sampling and provided data on chlorophyll and bacterial abundance in the North Sea. B.W., S.V., A.P. and R.D. carried out the genomic, metagenomic and metatranscriptomic analyses. L.G. and W.H.J. provided samples from various oceans. S.B. and M.S. wrote the major parts of the manuscript and all authors contributed to writing and revising it.

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Correspondence to Meinhard Simon.

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Supplementary Text, Supplementary Figures 1-4, Supplementary Tables 1-6 and 8-10, Supplementary Table 7 Legend and Supplementary References. (PDF 11314 kb)

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Billerbeck, S., Wemheuer, B., Voget, S. et al. Biogeography and environmental genomics of the Roseobacter-affiliated pelagic CHAB-I-5 lineage. Nat Microbiol 1, 16063 (2016). https://doi.org/10.1038/nmicrobiol.2016.63

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