DOI: 10.1073/pnas.0605127103. Microbial diversity in the deep sea and the underexplored “rare biosphere”

Microbial diversity in the deep sea and the underexplored “rare biosphere”

10.1073/pnas.0605127103

Crossref journal-article

Proceedings of the National Academy of Sciences

Proceedings of the National Academy of Sciences (341)

Abstract

The evolution of marine microbes over billions of years predicts that the composition of microbial communities should be much greater than the published estimates of a few thousand distinct kinds of microbes per liter of seawater. By adopting a massively parallel tag sequencing strategy, we show that bacterial communities of deep water masses of the North Atlantic and diffuse flow hydrothermal vents are one to two orders of magnitude more complex than previously reported for any microbial environment. A relatively small number of different populations dominate all samples, but thousands of low-abundance populations account for most of the observed phylogenetic diversity. This “rare biosphere” is very ancient and may represent a nearly inexhaustible source of genomic innovation. Members of the rare biosphere are highly divergent from each other and, at different times in earth's history, may have had a profound impact on shaping planetary processes.

Bibliography

Sogin, M. L., Morrison, H. G., Huber, J. A., Welch, D. M., Huse, S. M., Neal, P. R., Arrieta, J. M., & Herndl, G. J. (2006). Microbial diversity in the deep sea and the underexplored ârare biosphere.â Proceedings of the National Academy of Sciences, 103(32), 12115â12120.

Authors 8

Mitchell L. Sogin (first)
Hilary G. Morrison (additional)
Julie A. Huber (additional)
David Mark Welch (additional)
Susan M. Huse (additional)
Phillip R. Neal (additional)
Jesus M. Arrieta (additional)
Gerhard J. Herndl (additional)

References 45 Referenced 2,974

10.4319/lo.1980.25.5.0943
10.1128/aem.33.5.1225-1228.1977
10.1073/pnas.95.12.6578
R. M. Atlas, R. Bartha Microbial Ecology: Fundamentals and Applications (Benjamin/Cummings, Redwood City, CA, 1993). / Microbial Ecology: Fundamentals and Applications by Atlas R. M. (1993)
10.1126/science.276.5313.734
10.1128/aem.59.5.1294-1302.1993
10.1038/345060a0
10.1371/journal.pbio.0040095
10.1046/j.1462-2920.2000.00133.x
10.1126/science.1107851
10.1038/nature04435
10.1126/science.1120250
10.1126/science.1093857
10.1073/pnas.89.12.5685
10.1007/s00248-002-1067-3
10.1128/AEM.68.4.1585-1594.2002
10.1128/AEM.71.1.467-479.2005
10.1146/annurev.micro.57.030502.090759
10.1128/AEM.71.3.1501-1506.2005
10.1093/nar/25.17.3389
W. R. Pearson Methods Mol. Biol. 25, 365–389 (1994). / Methods Mol. Biol. by Pearson W. R. (1994)
10.1093/nar/gki038
A. Chao Scand. J. Stat. 11, 265–270 (1984). / Scand. J. Stat. by Chao A. (1984)
10.1080/01621459.1992.10475194
10.1093/biomet/80.1.193
10.1073/pnas.142680199
10.1016/S0168-6496(03)00257-5
10.1128/AEM.65.9.3982-3989.1999
10.1038/nature02649
10.1111/j.1462-2920.2004.00712.x
P. D. Hebert A. Cywinska S. L. Ball J. R. deWaard 270 313–321 (2003). (10.1098/rspb.2002.2218)
10.1038/nature03959
10.1093/bioinformatics/btg200
10.1093/nar/gkh293
10.1093/nar/gkj158
10.1128/AEM.67.10.4566-4572.2001
10.1111/j.1574-6941.2003.tb01080.x
10.1128/AEM.66.9.3798-3806.2000
K. Alain, J. Querellou, F. Lesongeur, P. Pignet, P. Crassous, G. Raguenes, V. Cueff, M. A. Cambon-Bonavita Int. J. Syst. Evol. Microbiol. 52, 1317–1323 (2002). (10.1099/00207713-52-4-1317) / Int. J. Syst. Evol. Microbiol. by Alain K. (2002)
10.1128/JB.187.9.3020-3027.2005
10.1128/AEM.71.11.7310-7320.2005
D. A. Butterfield, M. D. Lilley, J. A. Huber, K. K. Roe, R. W. Embley, J. A. Baross, G. J. Massoth The Subseafloor Biosphere at Mid-Ocean Ridges,, eds W. S. D. Wilcock, E. F. DeLong, D. S. Kelley, J. A. Baross, S. C. Cary (Am. Geophys. Union, Washington, DC), pp. 269–289, Vol. Geophysical Monograph 144. (2004). (10.1029/144GM17) / The Subseafloor Biosphere at Mid-Ocean Ridges, by Butterfield D. A. (2004)
10.1016/S0168-9525(00)02024-2
10.1186/1471-2105-5-113
10.1093/bioinformatics/18.11.1546

Dates

Type	When
Created	19 years, 1 month ago (Aug. 2, 2006, 3:50 a.m.)
Deposited	7 months, 3 weeks ago (Jan. 10, 2025, 3:38 a.m.)
Indexed	2 days, 19 hours ago (Sept. 3, 2025, 7:02 a.m.)
Issued	19 years ago (Aug. 8, 2006)
Published	19 years ago (Aug. 8, 2006)
Published Online	19 years ago (Aug. 8, 2006)
Published Print	19 years ago (Aug. 8, 2006)

Funders 0

None

BibTeX

@article{Sogin_2006, title={Microbial diversity in the deep sea and the underexplored “rare biosphere”}, volume={103}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.0605127103}, DOI={10.1073/pnas.0605127103}, number={32}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Sogin, Mitchell L. and Morrison, Hilary G. and Huber, Julie A. and Welch, David Mark and Huse, Susan M. and Neal, Phillip R. and Arrieta, Jesus M. and Herndl, Gerhard J.}, year={2006}, month=aug, pages={12115–12120} }

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