The abundant and diverse viruses of the seas

What is the most abundant biological entity in the oceans?

Viruses, of course! The quantity and diversity of viruses in the seas are staggering. Each milliliter of ocean water contains several million virus particles – a global total of 1030 virions! If lined up end to end, they would stretch 200 million light years into space. Viruses constitute 94% of all nucleic-acid containing particles in the sea and are 15 fold more abundant than bacteria and archaea.

Because viruses kill cells, they have a major impact on ocean ecology. About 1023 virus infections occur each second in the oceans; in surface waters they eliminate 20-40% of prokaryotes daily. Viral lysis converts living organisms into particulate matter that becomes carbon dioxide after respiration and photodegradation. Cell killing by viruses also liberates enough iron to supply the needs of phytoplankton, and leads to the production of dimethyl sulphoxide, a gas that influences the climate of the Earth. Because of these activities, marine viruses have a significant impact on global microbial communities and geothermal cycles.

Most of the marine viruses are bacteriophages, but there are also significant numbers that infect eukaryotic phytoplankton, invertebrates, and vertebrates. The best studied viruses are those that infect commercially important species. Novel viruses are frequently discovered; for example, white spot syndrome virus of panaeid shrimp is a member of a new virus family. Viruses of commercially important finfish include herpesviruses, reoviruses, nodaviruses, birnaviruses, and rhabdoviruses. How these viruses are transmitted among marine species is not understood. Many viruses move between marine and fresh waters, posing threats to fishing industries. The rhabdovirus viral hemorrhagic septicemia virus, which causes disease in European farmed trout, has been isolated from 40 marine fish species, from fish farms in Alaska, and from fish in the Great Lakes.

Many ocean viruses cause disease in marine mammals. Phocid distemper virus is a morbillivirus of Arctic phocid seals that has killed thousands of harbor seals in Europe. Similar viruses kill dolphins and other cetaceans. Many other viruses infect marine mammals and even cause disease in humans, including adenoviruses, herpesviruses, parvoviruses, and caliciviruses. The natural reservoirs of most of these viruses are unknown.

Massive sequencing projects have been used to provide information on the diversity of marine viruses. In these studies, seawater is filtered to remove large particles, virions are purified by centrifugation, and nucleic acids are extracted, amplified, and subjected to pyrosequencing. Bioinformatic approaches are used to sift through megabase data sets to identify viral sequences. In one study the viral genomes (‘viromes’) from the Arctic Ocean, the Sargasso Sea, and the coastal waters of British Columbia and the Gulf of Mexico were compared. Over 90% of the sequences were not found in the GenBank collection. There was also little sequence overlap among the samples from the four sites. Similar studies have revealed a rich array of RNA viruses in two different coastal environments; again, most of the sequences were not present in current databases. From the results of these studies it has been estimated that the oceans probably harbor several hundred thousand viral species.

Much more work is required to understand the diversity of marine viruses and their role in the global ecosystem. From the studies done to date, one conclusion is quite clear: the numbers of viruses in the oceans, and their impact on marine life, is far greater than we we ever imagined. And the zoonotic pool may be much larger than we suspected.

Suttle, C. (2007). Marine viruses — major players in the global ecosystem Nature Reviews Microbiology, 5 (10), 801-812 DOI: 10.1038/nrmicro1750

Angly, F., Felts, B., Breitbart, M., Salamon, P., Edwards, R., Carlson, C., Chan, A., Haynes, M., Kelley, S., Liu, H., Mahaffy, J., Mueller, J., Nulton, J., Olson, R., Parsons, R., Rayhawk, S., Suttle, C., & Rohwer, F. (2006). The Marine Viromes of Four Oceanic Regions PLoS Biology, 4 (11) DOI: 10.1371/journal.pbio.0040368

Culley, A., Lang, A.S., & Suttle, C.A. (2006). Metagenomic Analysis of Coastal RNA Virus Communities Science, 312 (5781), 1795-1798 DOI: 10.1126/science.1127404