Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Bacterial carbon processing by generalist species in the coastal ocean

Abstract

The assimilation and mineralization of dissolved organic carbon (DOC) by marine bacterioplankton is a major process in the ocean carbon cycle1. However, little information exists on the specific metabolic functions of participating bacteria and on whether individual taxa specialize on particular components of the marine DOC pool2. Here we use experimental metagenomics to show that coastal communities are populated by taxa capable of metabolizing a wide variety of organic carbon compounds. Genomic DNA captured from bacterial community subsets metabolizing a single model component of the DOC pool (either dimethylsulphoniopropionate or vanillate) showed substantial overlap in gene composition as well as a diversity of carbon-processing capabilities beyond the selected phenotypes. Our direct measure of niche breadth for bacterial functional assemblages indicates that, in accordance with ecological theory, heterogeneity in the composition and supply of organic carbon to coastal oceans may favour generalist bacteria. In the important interplay between microbial community structure and biogeochemical cycling, coastal heterotrophic communities may be controlled less by transient changes in the carbon reservoir that they process and more by factors such as trophic interactions and physical conditions.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Apparent taxonomic distribution of 16S rRNA-like gene sequences recovered from metagenomes.
Figure 2: Estimated genome equivalents in experimental metagenomic data sets based on homologue counts for single-copy genes.

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Data deposits

Metagenomic sequences are deposited in the Genome Projects Database (http://www.ncbi.nlm.nih.gov/Genomes) under accession number 19145. 16S rRNA gene sequences are deposited in GenBank under accession numbers DQ880941DQ881441 and EU167151EU167496.

References

  1. Azam, F. Microbial control of oceanic carbon flux: The plot thickens. Science 280, 694–696 (1998)

    Article  CAS  Google Scholar 

  2. Fuhrman, J. A. et al. Annually reoccurring bacterial communities are predictable from ocean conditions. Proc. Natl Acad. Sci. USA 103, 13104–13109 (2007)

    Article  ADS  Google Scholar 

  3. Cottrell, M. T. & Kirchman, D. L. Natural assemblages of marine proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter. Appl. Environ. Microbiol. 66, 1692–1697 (2000)

    Article  CAS  Google Scholar 

  4. Kiene, R. P., Linn, L. J. & Bruton, J. A. New and important roles for DMSP in marine microbial communities. J. Sea Res. 43, 209–224 (2000)

    Article  CAS  ADS  Google Scholar 

  5. Moran, M. A. & Hodson, R. E. Dissolved humic substances of vascular plant origin in a coastal marine environment. Limnol. Oceanogr. 39, 762–771 (1994)

    Article  CAS  ADS  Google Scholar 

  6. Urbach, E., Vergin, K. L. & Giovannoni, S. J. Immunochemical detection and isolation of DNA from metabolically active bacteria. Appl. Environ. Microbiol. 65, 1207–1213 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Hamasaki, K., Taniguchi, A., Tada, Y., Long, R. A. & Azam, F. Actively growing bacteria in the Inland Sea of Japan, identified by combined bromodeoxyuridine immunocapture and denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 73, 2787–2798 (2007)

    Article  CAS  Google Scholar 

  8. Crump, B. C., Armbrust, E. V. & Baross, J. A. Phylogenetic analysis of particle-attached and free-living bacterial communities in the Columbia River, its estuary, and the adjacent coastal ocean. Appl. Environ. Microbiol. 65, 3192–3204 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Santos, S. R. & Ochman, H. Identification and phylogenetic sorting of bacterial lineages with universally conserved genes and proteins. Environ. Microbiol. 6, 754–759 (2004)

    Article  CAS  Google Scholar 

  10. Howard, E. C. et al. Bacterial taxa limiting sulfur flux from the ocean. Science 314, 649–652 (2006)

    Article  CAS  ADS  Google Scholar 

  11. Todd, J. D. et al. Structural and regulatory genes required to make the gas dimethyl sulfide in bacteria. Science 315, 666–669 (2007)

    Article  CAS  ADS  Google Scholar 

  12. Buchan, A., Collier, L. S., Neidle, E. L. & Moran, M. A. Key aromatic-ring-cleaving enzyme, protocatechuate 3,4-dioxygenase, in the ecologically important marine Roseobacter lineage. Appl. Environ. Microbiol. 66, 4662–4672 (2000)

    Article  CAS  Google Scholar 

  13. Rodriguez-Brito, B., Rohwer, F. & Edwards, R. An application of statistics to comparative metagenomics. BMC Bioinformatics 7, 162 (2006)

    Article  Google Scholar 

  14. Edwards, R. A. et al. Using pyrosequencing to shed light on deep mine microbial ecology under extreme hydrogenologic conditions. BMC Genomics 7, 57 (2006)

    Article  Google Scholar 

  15. DeLong, E. F. et al. Community genomics among stratified microbial assemblages in the ocean’s interior. Science 311, 496–503 (2006)

    Article  CAS  ADS  Google Scholar 

  16. Yokokawa, T. & Nagata, T. Growth and grazing mortality rates of phylogenetic groups of bacterioplankton in coastal marine environments. Appl. Environ. Microbiol. 71, 6799–6807 (2005)

    Article  CAS  Google Scholar 

  17. Vila, M. et al. Use of microautoradiography combined with fluorescence in situ hybridization to determine dimethylsulfoniopropionate incorporation by marine bacterioplankton taxa. Appl. Environ. Microbiol. 70, 4648–4657 (2004)

    Article  CAS  Google Scholar 

  18. Kassen, R. The experimental evolution of specialists, generalists, and the maintenance of diversity. J. Evol. Biol. 15, 173–190 (2002)

    Article  Google Scholar 

  19. Futuyma, D. J. & Moreno, G. The evolution of ecological specialization. Annu. Rev. Ecol. Syst. 19, 207–233 (1988)

    Article  Google Scholar 

  20. Hutchinson, G. E. Concluding remarks. Quant. Biol. 22, 415–427 (1957)

    Article  Google Scholar 

  21. Moran, M. A., Sheldon, W. M. & Sheldon, J. E. Biodegradation of riverine dissolved organic carbon in five estuaries of the Southeastern United States. Estuaries 22, 55–64 (1999)

    Article  CAS  Google Scholar 

  22. Button, D. K., Robertson, B., Gustafson, E. & Zhao, X. Experimental and theoretical bases of specific affinity, a cytoarchitecture-based formulation of nutrient collection proposed to supercede the Michaelis–Menten paradigm of microbial kinetics. Appl. Environ. Microbiol. 70, 5511–5521 (2004)

    Article  CAS  Google Scholar 

  23. Bouvier, T. & del Giorgio, P. A. Key role of selective viral-induced mortality in determining marine bacterial community composition. Environ. Microbiol. 9, 287–297 (2007)

    Article  CAS  Google Scholar 

  24. Beardsley, C., Pernthaler, J., Wosniok, W. & Amann, R. Are readily culturable bacteria in coastal North Sea waters suppressed by selective grazing mortality? Appl. Environ. Microbiol. 69, 2624–2630 (2003)

    Article  CAS  Google Scholar 

  25. Hewson, I., Steele, J. A., Capone, D. G. & Fuhrman, J. A. Temporal and spatial scales of variation in bacterioplankton assemblages of oligotrophic surface waters. Mar. Ecol. Prog. Ser. 311, 67–77 (2006)

    Article  ADS  Google Scholar 

  26. Doney, S. C., Abbott, M. R., Cullen, J. J., Karl, D. M. & Rothstein, L. From genes to ecosystems: the ocean’s new frontier. Frontiers Ecol. Environ. 2, 457–468 (2004)

    Article  Google Scholar 

  27. Follows, M. J., Dutkiewicz, S., Grant, S. & Chisholm, S. W. Emergent biogeography of microbial communities in a model ocean. Science 315, 1843–1846 (2007)

    Article  CAS  ADS  Google Scholar 

  28. Su, Z. et al. Computational inference and experimental validation of the nitrogen assimilation regulatory network in cyanobacterium Synechococcus sp. WH 8102. Nucleic Acids Res. 34, 1050–1065 (2006)

    Article  CAS  Google Scholar 

  29. Moran, M. A. et al. Genome sequence of Silicibacter pomeroyi reveals adaptations to the marine environment. Nature 432, 910–913 (2004)

    Article  CAS  ADS  Google Scholar 

  30. Yutin, N. et al. Assessing diversity and biogeography of aerobic anoxygenic phototrophic bacteria in surface waters of the Atlantic and Pacific Oceans using the Global Ocean Sampling expedition metagenomes. Environ. Microbiol. 9, 1464–1475 (2007)

    Article  CAS  Google Scholar 

  31. Urbach, E., Vergin, K. L. & Giovannoni, S. J. Immunochemical detection and isolation of DNA from metabolically active bacteria. Appl. Environ. Microbiol. 65, 1207–1213 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Moran, M. A. et al. Genome sequence of Silicibacter pomeroyi reveals adaptations to the marine environment. Nature 432, 910–913 (2004)

    Article  CAS  ADS  Google Scholar 

  33. Tatusov, R. L. et al. The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res. 29, 22–28 (2001)

    Article  CAS  Google Scholar 

  34. Kanehisa, M. & Goto, S. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 28, 27–30 (2000)

    Article  CAS  Google Scholar 

  35. Overbeek, R. et al. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res. 33, 5691–5702 (2005)

    Article  CAS  Google Scholar 

  36. Rodriguez-Brito, B., Rohwer, F. & Edwards, R. An application of statistics to comparative metagenomics. BMC Bioinform. 7, 162 (2006)

    Article  Google Scholar 

  37. Delong, E. F., Wickham, G. S. & Pace, N. R. Phylogenetic stains—ribosomal RNA-based probes for the identification of single cells. Science 243, 1360–1363 (1989)

    Article  CAS  ADS  Google Scholar 

  38. Ashelford, K. E. et al. 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  CAS  Google Scholar 

  39. Kumar, S., Tamura, K. & Nei, M. MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform. 5, 150–163 (2004)

    Article  CAS  Google Scholar 

  40. Schloss, P. D. & Handelsman, J. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl. Environ. Microbiol. 71, 1501–1506 (2005)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank W. Whitman, C. Lasher, B. Rodriguez-Brito, C. Reisch, J. Henriksen, E. Biers and W. Sheldon for advice or assistance with experimental or bioinformatic analyses; C. English for graphics; and J. T. Hollibaugh for discussions. This project was funded by grants from the National Science Foundation and the Gordon and Betty Moore Foundation.

Author Contributions X.M. and M.A.M. planned the project; X.M. conducted the experimental work; S.S. and R.A.E. conducted the bioinformatic and statistical analyses; X.M., R.E.H. and M.A.M. interpreted results; M.A.M. directed the project and wrote the paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mary Ann Moran.

Supplementary information

Supplementary Information

This file contains Supplementary Tables S1-S3 and Supplementary Figures S1-S13 with Legends. (PDF 1698 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mou, X., Sun, S., Edwards, R. et al. Bacterial carbon processing by generalist species in the coastal ocean. Nature 451, 708–711 (2008). https://doi.org/10.1038/nature06513

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature06513

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing