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Biodiversity and biogeography of phages in modern stromatolites and thrombolites

Nature volume 452, pages 340–343 (2008)Cite this article

Abstract

Viruses, and more particularly phages (viruses that infect bacteria), represent one of the most abundant living entities in aquatic and terrestrial environments. The biogeography of phages has only recently been investigated and so far reveals a cosmopolitan distribution of phage genetic material (or genotypes)1,2,3,4. Here we address this cosmopolitan distribution through the analysis of phage communities in modern microbialites, the living representatives of one of the most ancient life forms on Earth. On the basis of a comparative metagenomic analysis of viral communities associated with marine (Highborne Cay, Bahamas) and freshwater (Pozas Azules II and Rio Mesquites, Mexico) microbialites, we show that some phage genotypes are geographically restricted. The high percentage of unknown sequences recovered from the three metagenomes (>97%), the low percentage similarities with sequences from other environmental viral (n = 42) and microbial (n = 36) metagenomes, and the absence of viral genotypes shared among microbialites indicate that viruses are genetically unique in these environments. Identifiable sequences in the Highborne Cay metagenome were dominated by single-stranded DNA microphages that were not detected in any other samples examined, including sea water, fresh water, sediment, terrestrial, extreme, metazoan-associated and marine microbial mats. Finally, a marine signature was present in the phage community of the Pozas Azules II microbialites, even though this environment has not been in contact with the ocean for tens of millions of years. Taken together, these results prove that viruses in modern microbialites display biogeographical variability and suggest that they may be derived from an ancient community.

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Figure 1: The phage proteomic tree.
Figure 2: Phylogenetic relationships among viral capsid amino-acid sequences of microphages.

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Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Data deposits

The microbialite viral metagenomes have been deposited into the ftp server of the SEED public database ftp://ftp.theseed.org/metagenomes under the project accession numbers 4440323.3(Highborne Cay), 4440320.3 (Pozas Azules II) and 4440321.3 (Rio Mesquites). The metagenomes are also publicly accessible in the CAMERA metagenomic database (http://camera.calit2.net) under the project accession numbers HBCStromBahamasVir011105 (Highborne Cay), PAStromCCMexVir072205 (Pozas Azules II), and RMStromCCMexVir072205 (Rio Mesquites). The Vp1 cloned sequences from the Highborne Cay sample have been deposited in GenBank under accession numbers EF679227 to EF679234.

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Acknowledgements

Logistical field support was provided by the crew of the RV Walton Smith, Highborne Cay management and personnel of the Area de Proteccion de Flora y Fauna of Cuatro Ciénegas. This work was supported by an NSF grant to F.R. Support for B.K.S. and D.L.V. was provided by the NSF. M.B. was supported by a grant from the University of South Florida's Internal New Research Awards Program. V.S. was funded by the CONACYT 2002-C01-0237 project. The authors thank P. Visscher, K. Przekop, L. Rothschild, D. Rogoff, V. Michotey, P. Bonin, S. Norman and E. Bowlin for providing samples of marine microbial mats and M. Schaechter for a critical reading of the manuscript.

Author Contributions C.D. and F.R. designed the project. C.D. analysed most of the bioinformatic results, conducted the molecular biology and wrote the article. S.K. performed the bayesian analysis. S.R. implemented the cross-contig analyses. M.H. extracted viral DNAs. B.R.-B., H.L., F.E.A. and R.A.E. performed bioinformatic analyses. R.V.T. and D.H. helped with the interpretation of the bioinformatic results. V.S., M.B., J.S. and R.P.R. collected the samples. B.K.S., D.L.V., M.F., T.T., L.L., Y.R., L.W. and B.C. provided metagenomic data. F.R. supervised the project and helped with the writing. All authors edited and commented on the manuscript.

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Authors and Affiliations

  1. Department of Biology,,

    Christelle Desnues, Beltran Rodriguez-Brito, Steve Rayhawk, Scott Kelley, Tuong Tran, Matthew Haynes, Hong Liu, Mike Furlan, Linda Wegley, Betty Chau, Dana Hall, Florent E. Angly, Robert A. Edwards, Linlin Li, Rebecca Vega Thurber & Forest Rohwer

  2. Computational Sciences Research Center,,

    Beltran Rodriguez-Brito, Steve Rayhawk & Robert A. Edwards

  3. Center for Microbial Sciences, San Diego State University, San Diego, California 92182, USA,

    Scott Kelley, Robert A. Edwards & Forest Rohwer

  4. Genome Institute of Singapore, Singapore 138672, Singapore

    Yijun Ruan

  5. Mathematics and Computer Science Division, Argonne National Laboratory, Argonne, Illinois 60439, USA,

    Robert A. Edwards

  6. Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, Florida 33149, USA,

    R. Pamela Reid

  7. Department of Statistics, Rice University, Houston, Texas 77251, USA,

    Janet Siefert

  8. Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autónoma de México AP 70-275 Coyoacán, 04510 Mexico D.F., Mexico

    Valeria Souza

  9. Department of Earth Science, University of California Santa Barbara, Santa Barbara, California 93106, USA,

    David L. Valentine & Brandon K. Swan

  10. College of Marine Science, University of South Florida, St Petersburg, Florida 33701, USA,

    Mya Breitbart

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Corresponding author

Correspondence to Christelle Desnues.

Supplementary information

Supplementary Information

The file contains Supplementary Figures 1-8 and Supplementary Tables 1-5 with Legends (Part 1); the viral capsid sequences reconstructed from the metagenomes (Part 2); and the sequences obtained from the cloning experiment with accession numbers (Part 3). (PDF 1315 kb)

Supplementary Video 1

The file contains Supplementary Video 1 describing the microbialites. (MOV 5481 kb)

Supplementary Video 2

The file contains Supplementary Video 2. The movie provides information on the sampling site in the Cuatro Ciénegas Basin (Mexico). (MOV 5854 kb)

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Desnues, C., Rodriguez-Brito, B., Rayhawk, S. et al. Biodiversity and biogeography of phages in modern stromatolites and thrombolites. Nature 452, 340–343 (2008). https://doi.org/10.1038/nature06735

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