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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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.
Angly, F. E. et al. The marine viromes of four oceanic regions. PLoS Biol. 4, e368 (2006)
Casas, V. et al. Widespread occurrence of phage-encoded exotoxin genes in terrestrial and aquatic environments in Southern California. FEMS Microbiol. Lett. 261, 141–149 (2006)
Breitbart, M., Miyake, J. H. & Rohwer, F. Global distribution of nearly identical phage-encoded DNA sequences. FEMS Microbiol. Lett. 236, 249–256 (2004)
Short, C. M. & Suttle, C. A. Nearly identical bacteriophage structural gene sequences are widely distributed in both marine and freshwater environments. Appl. Environ. Microbiol. 71, 480–486 (2005)
Walter, M. R. Stromatolites. (Elsevier, Amsterdam, 1976)
Allwood, A. C., Walter, M. R., Kamber, B. S., Marshall, C. P. & Burch, I. W. Stromatolite reef from the Early Archaean era of Australia. Nature 441, 714–718 (2006)
Schopf, J. W. Fossil evidence of Archaean life. Phil. Trans. R. Soc. Lond. B 361, 869–885 (2006)
Suttle, C. A. Viruses in the sea. Nature 437, 356–361 (2005)
Cho, J. C. & Tiedje, J. M. Biogeography and degree of endemicity of fluorescent Pseudomonas strains in soil. Appl. Environ. Microbiol. 66, 5448–5456 (2000)
Papke, R. T., Ramsing, N. B., Bateson, M. M. & Ward, D. M. Geographical isolation in hot spring cyanobacteria. Environ. Microbiol. 5, 650–659 (2003)
Whitaker, R. J., Grogan, D. W. & Taylor, J. W. Geographic barriers isolate endemic populations of hyperthermophilic Archaea. Science 301, 976–978 (2003)
Whitaker, R. J. Allopatric origins of microbial species. Phil. Trans. R. Soc. Lond. B 361, 1975–1984 (2006)
Sano, E., Carlson, S., Wegley, L. & Rohwer, F. Movement of viruses between biomes. Appl. Environ. Microbiol. 70, 5842–5846 (2004)
Breitbart, M. & Rohwer, F. Here a virus, there a virus, everywhere the same virus? Trends Microbiol. 13, 278–284 (2005)
Breitbart, M. et al. Genomic analysis of uncultured marine viral communities. Proc. Natl Acad. Sci. USA 99, 14250–14255 (2002)
Rohwer, F. & Edwards, R. A. The phage proteomic tree: a genome-based taxonomy for phage. J. Bacteriol. 184, 4529–4535 (2002)
Fane, B. Microviridae, in Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses. (eds Fauquet, M. A. M. C., Maniloff, J., Desselberger, U. & Ball, L. A.) 289–299 (Elsevier Academic Press, San Diego, California, 2005)
Souza, V. et al. An endangered oasis of aquatic microbial biodiversity in the Chihuahuan desert. Proc. Natl Acad. Sci. USA 103, 6565–6570 (2006)
Sambrook, J., Fritsch, E. F. & Maniatis, T. Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor Laboratory Press, New York, 1989)
Margulies, M. et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437, 376–380 (2005)
Lozupone, C., Hamady, M. & Knight, R. UniFrac - An online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7, 371 (2006)
Jensen, J., Bohonak, A. & Kelley, S. Isolation by distance, web service. BMC Genet. 6, 13 (2005)
Reid, R. P., Macintyre, I. G. & Steneck, R. S. A microbialite/algal ridge fringing reef complex, Highborne Cay, Bahamas. Atoll Res. Bull. 465, 1–18 (1999)
Chen, F., Lu, J., Binder, B. J., Liu, Y. & Hodson, R. E. Application of digital image analysis and flow cytometry to enumerate marine viruses stained with SYBR Gold. Appl. Environ. Microbiol. 67, 539–545 (2001)
Altschul, S. F., Gish, W., Miller, W., Meyers, E. W. & Lipman, D. J. Basic Local Alignment Search Tool. J. Mol. Biol. 215, 403–410 (1990)
Angly, F. et al. PHACCS, an online tool for estimating the structure and diversity of uncultured viral communities using metagenomic information. BMC Bioinformatics 6, 41 (2005)
Thompson, J. D., Higgins, D. G. & Gibson, T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680 (1994)
Huelsenbeck, J. P. & Ronquist, F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755 (2001)
Saito, N. & Nei, M. The neighbour-joining method, a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 79, 426–434 (1987)
Perriere, G. & Gouy, M. WWW-Query: An on-line retrieval system for biological sequence banks. Biochimie 78, 364–369 (1996)
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.
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)
The file contains Supplementary Video 1 describing the microbialites. (MOV 5481 kb)
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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