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Fine-scale phylogenetic architecture of a complex bacterial community

Abstract

Although molecular data have revealed the vast scope of microbial diversity1, two fundamental questions remain unanswered even for well-defined natural microbial communities: how many bacterial types co-exist, and are such types naturally organized into phylogenetically discrete units of potential ecological significance? It has been argued that without such information, the environmental function, population biology and biogeography of microorganisms cannot be rigorously explored2. Here we address these questions by comprehensive sampling of two large 16S ribosomal RNA clone libraries from a coastal bacterioplankton community. We show that compensation for artefacts generated by common library construction techniques reveals fine-scale patterns of community composition. At least 516 ribotypes (unique rRNA sequences) were detected in the sample and, by statistical extrapolation, at least 1,633 co-existing ribotypes in the sampled population. More than 50% of the ribotypes fall into discrete clusters containing less than 1% sequence divergence. This pattern cannot be accounted for by interoperon variation, indicating a large predominance of closely related taxa in this community. We propose that such microdiverse clusters arise by selective sweeps and persist because competitive mechanisms are too weak to purge diversity from within them.

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Figure 1: Compositional pattern of the coastal bacterioplankton sample.
Figure 2: Phylogenetic distance relationships between the coastal bacterioplankton based on partial 16S rRNA sequencing.

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References

  1. Rappé, M. S. & Giovannoni, S. J. The uncultured microbial majority. Annu. Rev. Microbiol. 57, 369–394 (2003)

    Article  PubMed  Google Scholar 

  2. Curtis, T. P., Sloan, W. T. & Scannell, J. W. Estimating prokaryotic diversity and its limits. Proc. Natl Acad. Sci. USA 99, 10494–10499 (2002)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  3. Rosselló-Mora, R. & Amann, R. The species concept for prokaryotes. FEMS Microbiol. Rev. 25, 39–67 (2001)

    Article  PubMed  Google Scholar 

  4. Cohan, F. M. What are bacterial species. Annu. Rev. Microbiol. 56, 457–487 (2002)

    Article  CAS  PubMed  Google Scholar 

  5. Palys, T., Nakamura, L. K. & Cohan, F. M. Discovery and classification of ecological diversity in the bacterial world: the role of DNA sequence data. Int. J. Syst. Bacteriol. 47, 1145–1156 (1997)

    Article  CAS  PubMed  Google Scholar 

  6. Venter, C. J. et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66–74 (2004)

    Article  ADS  CAS  PubMed  Google Scholar 

  7. Hughes, J. B., Hellmann, J. J., Ricketts, T. H. & Bohannan, B. J. M. Counting the uncountable: statistical approaches to estimating microbial diversity. Appl. Environ. Microbiol. 67, 4399–4406 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Martin, A. P. Phylogenetic approaches for describing and comparing the diversity of microbial communities. Appl. Environ. Microbiol. 68, 3673–3682 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Acinas, S. G., Marcelino, L. A., Klepac-Ceraj, V. & Polz, M. F. Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons. J. Bacteriol. 186, 2629–2635 (2004)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Klappenbach, J. A., Dunbar, J. M. & Schmidt, T. M. rRNA operon copy number reflects ecological strategies of bacteria. Appl. Environ. Microbiol. 66, 1328–1333 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Hacker, J. & Carniel, E. Ecological fitness, genomic islands and bacterial pathogenicity—a Darwinian view of the evolution of microbes. EMBO Rep. 2, 376–381 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Lan, R. T. & Reeves, P. R. When does a clone deserve a name? A perspective on bacterial species based on population genetics. Trends Microbiol. 9, 419–424 (2001)

    Article  CAS  PubMed  Google Scholar 

  13. Welch, R. A. et al. Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc. Natl Acad. Sci. USA 99, 17020–17024 (2002)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  14. Daubin, V., Moran, N. A. & Ochman, H. Phylogenetics and the cohesion of bacterial genomes. Science 301, 829–832 (2003)

    Article  ADS  CAS  PubMed  Google Scholar 

  15. Rocap, G. et al. Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424, 1042–1047 (2003)

    Article  ADS  CAS  PubMed  Google Scholar 

  16. Schleper, C. A. et al. Genomic analysis reveals chromosomal variation in natural populations of the uncultured psychrophilic archaeon Crenarchaeum symbiosum. J. Bacteriol. 180, 5003–5009 (1998)

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Béja, O. et al. Comparative genomic analysis of archaeal genotypic variants in a single population and in two different oceanic provinces. Appl. Environ. Microbiol. 68, 335–345 (2002)

    Article  PubMed  PubMed Central  Google Scholar 

  18. Thingstad, T. F. Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol. Oceanogr. 45, 1320–1328 (2000)

    Article  ADS  Google Scholar 

  19. Lan, R. T. & Reeves, P. R. Intraspecies variation in bacterial genomes: the need for a species genome concept. Trends Microbiol. 8, 396–401 (2000)

    Article  CAS  PubMed  Google Scholar 

  20. Klepac-Ceraj, V. et al. High overall diversity and dominance of microdiverse relationships in salt marsh sulfate-reducing bacteria. Environ. Microbiol. doi: 10.1111/j.1462–2920.2004.00600.x (2004)

  21. Connon, S. A. & Giovannoni, S. J. High-throughput method for culturing microorganisms in very low nutrient media yield diverse new marine isolates. Appl. Environ. Microbiol. 768, 3878–3885 (2002)

    Article  Google Scholar 

  22. Vergin, K. L. et al. Screening of a fosmid library of marine environmental genomic DNA fragments reveals four clones related to members of the order Planctomycetales. Appl. Environ. Microbiol. 64, 3075–3078 (1998)

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Thompson, J. R., Marcelino, L. A. & Polz, M. F. Heteroduplexes in mixed-template amplifications: formation, consequences and elimination by ’reconditioning PCR’. Nucleic Acids Res. 30, 2083–2088 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Cole, J. R. et al. The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res. 31, 442–443 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Hugenholtz, P. & Huber, T. Chimeric 16S rDNA sequences of diverse origin are accumulating in the public databases. Int. J. Syst. Evol. Microbiol. 53, 289–293 (2003)

    Article  CAS  PubMed  Google Scholar 

  26. Field, K. G. et al. Diversity and depth-specific distribution of SAR11 cluster rRNA genes from marine planktonic bacteria. Appl. Environ. Microbiol. 63, 63–70 (1997)

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Pybus, O. G. & Rambaut, A. GENIE: Estimating demographic history from molecular phylogenies. Bioinformatics 18, 1404–1405 (2003)

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Swofford, D. L. PAUP*. Phylogenetic Analysis Using Parsimony (*And Other Methods) Version 4 (Sinauer Associates, Sunderland, Massachusetts, 2002)

    Google Scholar 

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Acknowledgements

We thank S. Bertilsson (Uppsala University) for sample collection, D. Veneziano (MIT) for discussions on statistical extrapolation of sequence diversity, P. Chisholm (MIT) for numerous suggestions, and researchers and staff of the PIE-LTER (Plum Island Ecosystem-Long Term Ecological Research) for logistical support. This work was supported by grants from the National Science Foundation, the Department of Energy Genomes to Life program and a postdoctoral fellowship from the Spanish Ministry of Education to S.G.A.

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Correspondence to Martin F. Polz.

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The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Figure 1

Phylogenetic distance (neighbour-joining) tree of all unique 16S rRNA gene sequences (ribotypes) retrieved from the Plum Island bacterioplankton sample and representative reference sequences. (PDF 33 kb)

Supplementary Figure Legend

Key to cluster numbers from Figure 2a in main paper. (RTF 4 kb)

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Acinas, S., Klepac-Ceraj, V., Hunt, D. et al. Fine-scale phylogenetic architecture of a complex bacterial community. Nature 430, 551–554 (2004). https://doi.org/10.1038/nature02649

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