1. Department of Biology,
2. Computational Sciences Research Center,
3. Center for Microbial Sciences, San Diego State University, San Diego, California 92182, USA
4. Genome Institute of Singapore, Singapore 138672, Singapore
5. Mathematics and Computer Science Division, Argonne National Laboratory, Argonne, Illinois 60439, USA
6. Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, Florida 33149, USA
7. Department of Statistics, Rice University, Houston, Texas 77251, USA
8. Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autónoma de México AP 70-275 Coyoacán, 04510 Mexico D.F., Mexico
9. Department of Earth Science, University of California Santa Barbara, Santa Barbara, California 93106, USA
10. College of Marine Science, University of South Florida, St Petersburg, Florida 33701, USA

Correspondence to: Christelle Desnues¹ Correspondence and requests for materials should be addressed to C.D. (Email: cdesnues@yahoo.fr).

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.