Expanding the marine virosphere using metagenomics

PLoS Genet. 2013;9(12):e1003987. doi: 10.1371/journal.pgen.1003987. Epub 2013 Dec 12.


Viruses infecting prokaryotic cells (phages) are the most abundant entities of the biosphere and contain a largely uncharted wealth of genomic diversity. They play a critical role in the biology of their hosts and in ecosystem functioning at large. The classical approaches studying phages require isolation from a pure culture of the host. Direct sequencing approaches have been hampered by the small amounts of phage DNA present in most natural habitats and the difficulty in applying meta-omic approaches, such as annotation of small reads and assembly. Serendipitously, it has been discovered that cellular metagenomes of highly productive ocean waters (the deep chlorophyll maximum) contain significant amounts of viral DNA derived from cells undergoing the lytic cycle. We have taken advantage of this phenomenon to retrieve metagenomic fosmids containing viral DNA from a Mediterranean deep chlorophyll maximum sample. This method allowed description of complete genomes of 208 new marine phages. The diversity of these genomes was remarkable, contributing 21 genomic groups of tailed bacteriophages of which 10 are completely new. Sequence based methods have allowed host assignment to many of them. These predicted hosts represent a wide variety of important marine prokaryotic microbes like members of SAR11 and SAR116 clades, Cyanobacteria and also the newly described low GC Actinobacteria. A metavirome constructed from the same habitat showed that many of the new phage genomes were abundantly represented. Furthermore, other available metaviromes also indicated that some of the new phages are globally distributed in low to medium latitude ocean waters. The availability of many genomes from the same sample allows a direct approach to viral population genomics confirming the remarkable mosaicism of phage genomes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actinobacteria / genetics
  • Actinobacteria / virology
  • Bacteriophages / genetics*
  • Cyanobacteria / genetics
  • Cyanobacteria / virology
  • DNA, Viral / genetics
  • DNA, Viral / isolation & purification
  • High-Throughput Nucleotide Sequencing*
  • Metagenomics*
  • Molecular Sequence Data
  • Prokaryotic Cells / virology*
  • Seawater / microbiology
  • Seawater / virology
  • Sequence Analysis, DNA


  • DNA, Viral

Associated data

  • GENBANK/AP014505
  • SRA/PRJNA210529

Grants and funding

This work was supported by projects MAGYK (BIO2008-02444), MICROGEN (Programa CONSOLIDER-INGENIO 2010 CDS2009-00006), CGL2009-12651-C02-01 from the Spanish Ministerio de Ciencia e Innovación, DIMEGEN (PROMETEO/2010/089) and ACOMP/2009/155 from the Generalitat Valenciana and MaCuMBA Project 311975 of the European Commission FP7. FEDER funds supported this project. RG was supported by a Juan de la Cierva scholarship from the Spanish Ministerio de Ciencia e Innovación. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.