Introduction to marine viruses
Marine viruses and their consequences
Viruses are an integral part of the marine ecosystem. As we assume to be true of all life on our planet, every living thing in the ocean appears to be susceptible to disease and death caused by viral infections. Although viruses cannot replicate autonomously, they outnumber all forms of cellular life in the oceans by roughly an order of magnitude (Maranger & Bird, 1995). The concentration of free virions in seawater (i.e. the marine virioplankton) is typically billions to tens-of-billions per liter at the surface (Bergh et al., 1989; Wommack & Colwell, 2000). The concentration of virioplankton does decline with depth, but they appear to be ubiquitous and are found deep in the ocean's interior (Cochlan et al., 1993; Hara et al., 1996; Ortmann & Suttle, 2005), yielding an estimated total abundance of >1030 in the sea (Suttle, 2005).
The virioplankton are not only numerous, but also extraordinarily diverse, both morphologically (Frank & Moebus, 1987; Weinbauer, 2004) and genetically (Edwards & Rohwer, 2005). Analyses of environmental shotgun clone libraries suggest that there may be a few thousand to perhaps 10 000 viral genotypes in samples from individual marine habitats (Breitbart et al., 2002; Bench et al., 2007). When seawater from four distinct oceanic regions was analysed, it was estimated that more than 50 000 genotypes were present among the samples (Angly et al., 2006).
Viruses can be a major source of disease and mortality for marine life. Epidemic infections have caused occasional mass mortalities of marine mammals (Geraci et al., 1982; Jensen et al., 2002) and fish (Skall et al., 2005), and some data suggest that viruses might have a role in coral bleaching (Wilson et al., 2001; Davy et al., 2006; Lohr et al., 2007). Marine viruses can even influence human health and prosperity. Epidemic viral infections of commercially exploited marine animals such as salmonids, shrimp, abalone, and oysters (Hasson et al., 1995; Friedman et al., 2005; McLoughlin & Graham, 2007), for example, can cause significant economic hardship. The ocean is also a reservoir of viruses that can infect terrestrial organisms (Sano et al., 2004), including humans (Smith et al., 1998a, b).
Viruses have been implicated in the natural termination of plankton blooms, some of which occur on a massive scale. For example, the marine coccolithophorid Emiliania huxleyi is capable of forming blooms in temperate waters that cover upwards of 10 000 km2, and viruses have been identified as the primary agent of E. huxleyi bloom termination in several instances (Bratbak et al., 1993, 1996; Brussaard et al., 1996; Jacquet et al., 2002; Wilson et al., 2002). Viruses have also been found in association with bloom termination events in other systems (Nagasaki et al., 1994; Tarutani et al., 2000; Tomaru et al., 2004a; Baudoux et al., 2006).
Viruses play an important role in the cycling of nutrients in the ocean through their infection and lysis of marine microorganisms. The overall effect of this viral activity is to augment the rate of movement of nutrients from particulate organic matter to dissolved organic matter, diverting nutrients from higher trophic levels back into the microbial fraction (Fuhrman, 1992; Suttle, 2007). Viruses also appear to promote diversity in planktonic communities (Van Hannen et al., 1999; Weinbauer & Rassoulzadegan, 2004; Bouvier & del Giorgio, 2007). One explanation is that, because viral infections are often host specific and the spread of an infection is density dependent, viruses tend to ‘kill the winner’ (Thingstad et al., 1993) and prevent the dominance of a single species. The release of diverse organic substrates from lysed cells that can be readily used by other bacteria appears to be a complementary process promoting diversity (Middelboe et al., 2003).
In addition to controlling the balance among existing species, viruses create new diversity by driving evolution of life on land and in the sea (Villarreal, 2005). The influence of viruses on evolutionary processes is particularly evident among the bacteria. Analyses of microbial genome sequences show that viruses actively modify bacterial genomes and that gene exchange between virus and host is a common occurrence (Canchaya et al., 2003a, b; Casjens, 2003).
The contribution of RNA viruses to the virioplankton
Since the first direct counts of viruses in seawater revealed their extraordinary abundance nearly two decades ago, the question of what contribution RNA viruses make to the virioplankton has been virtually ignored. A number of lines of indirect evidence have been used to argue that most of the viruses constituting the marine virioplankton have DNA genomes (Steward et al., 1992; Weinbauer, 2004). The actual numerical contribution of RNA viruses to the marine virioplankton has remained rather poorly constrained, however, because of methodological limitations. Routine staining procedures for electron microscopy do not distinguish the nucleic acid content of viral particles (Fig. 1), while flow cytometry and epifluorescence microscopy (Fig. 2) appear to the lack the sensitivity, at present, to accurately enumerate viruses with small genomes containing either RNA or DNA (Brussaard et al., 2000; Tomaru & Nagasaki, 2007).
Despite uncertainties about their abundance, RNA viruses are diverse and ecologically important. RNA viruses of every major classification (single- and double-stranded, positive- and negative-sense), and which infect a diverse range of host species, have been isolated from the sea (Table 1). Diseases caused by RNA viruses can have devastating effects on populations of aquatic animals. The causes and consequences are best understood for farmed aquatic animals where factors such as high-density culture, substandard environmental conditions and nonregulated movement of animals can increase the risk and incidence of viral disease outbreaks. Molecular biology and genomic methods are rapidly advancing the study of host and pathogen genomes and the molecular mechanisms involved in host–pathogen interactions in marine fish and shellfish (e.g. von Schalburg et al., 2005; Purcell et al., 2006; Rattanarojpong et al., 2007; Poisa-Beiro et al., 2008; Rise et al., 2008). These studies promise to aid in the development of new diagnostics for identifying viral pathogens in animal tissues and water samples, novel approaches and models for studying the dissemination and evolution of marine RNA viruses, and tools such as vaccines and therapeutics for preventing outbreaks of viral diseases in populations of farmed aquatic animals. Because they are of immediate practical concern, RNA viruses infecting commercially exploited shellfish and fish species, and those infecting marine mammals, have already received considerable attention. In contrast, most of what we know about RNA viruses infecting unicellular marine plankton has been learned only in the past 5 years. However, this work is clearly demonstrating important linkages between host species dynamics and viral abundances in natural environments.
|Viruses||Host species||Properties and comments|
|Positive-sense ssRNA viruses|
|HaRNAV||Heterosigma akashiwo (protist)||8.6-kb genome, monocistronic; Fig. 4|
|TSV||Penaeid shrimp||10.2-kb genome, dicistronic; Fig. 6|
Serious impacts on aquaculture
|SePV-1||Ringed seal (Phoca hispida)||6.7-kb genome, monocistronic|
Likely a new genus
|SMSV||Marine mammals, humans, invertebrates, fish||8.3-kb genome, polycistronic; Fig. 6|
|WCV||Walrus (Odobenus rosmarus)|
|RCV||California sea lion (Zalophus californianus), Steller sea lion (Eumetopias jubatus)|
|Unidentified||Fish, white tern (Gygis alba)|
|Nodaviridae||3.1- and 1.4-kb bisegmented genome|
|BFNNV, ACNNV, DIEV, JFNNV, LcEV, RGNNV, SJNNV, TPNNV||Numerous fish species [e.g. barfin flounder (Verasper moseri), Atlantic cod (Gadus morhua) tiger puffer (Takifugu rubripes), Japanese flounder (Paralichthys olivaceus)]||Widely distributed with serious impacts on aquaculture|
|PvNV||Penaeus vannamei (shrimp)|
|SPDV/SAV1||Atlantic salmon (Salmo salar)||11.9-kb genome, dicistronic; Fig. 6; enveloped|
Serious impacts on aquaculture; transmission by sea lice?
|NSAV/SAV3||Atlantic salmon, rainbow trout (Oncorhynchus mykiss)|
|SES||Louse (Lepidopthirus macrorhini), southern elephant seal (Mirounga leonina)|
|YHV||Various species of shrimp, prawns and krill||c. 26-kb genome, polycistronic; enveloped|
Serious impacts on shrimp aquaculture
|TYUV||Tufted puffin (Fratercula cirrhata), common murre (Uria aalge), thick-billed murre (U. lomvia)||c. 11 kb genome, monocistronic; enveloped|
|HcRNAV||Heterocapsa circularisquama (protist)||4.4-kb genome, dicistronic; Fig. 4|
|RsRNAV||Rhizosolenia setigera (protist)||8.9-kb genome, dicistronic; Fig. 4|
Likely in order Picornavirales
|CtenRNAV||Chaetoceros tenuissimus (protist)||9.4-kb genome, dicistronic|
Likely in order Picornavirales
|SssRNAV||Aurantiochytrium sp. (protist)||9-kb genome, polycistronic; Fig. 4|
Likely in order Picornavirales
|LSNV||Black tiger shrimp (Penaeus monodon)||Presumed to be positive-sense based on phylogenetic affiliations|
|CsfrRNAV||Chaetoceros socialis (protist)||(Sense unknown)|
|06N-58P||Pseudomonas sp.||60 nm enveloped particle (sense unknown)|
|JP-A||Unknown (protist?)||Complete genome assembled from environment; presumed to be protist-infecting and positive-sense based on phylogenetic affiliations|
|JP-B||Unknown (protist?)||Complete genome assembled from environment; presumed to be protist-infecting and positive-sense based on phylogenetic affiliations|
|SOG||Unknown||Complete genome assembled from environment; most closely related to family Tombusviridae; presumed to be positive-sense based on phylogenetic affiliations|
|Negative-sense ssRNA viruses|
|ISAV||Atlantic salmon, sea trout (Salmo trutta), Arctic char (Salvelinus alpinus), herring (Clupea harengus)||Eight segments (from 0.9 to 2.4 kb) with 12.7 kb total genome; enveloped|
|Influenza A||Marine mammals [e.g. harbor seal (Phoca vitulina), pilot whales (Globicephala melaena)], many birds, humans||Eight segments (from 0.9 to 2.4 kb) with 13.6 kb total genome; enveloped|
|Paramyxoviridae||c. 15-kb genome, polycistronic; enveloped|
|PDV||Various marine mammals||Serious impacts on seal populations|
|CeMV||Various marine mammals|
|Rhabdoviridae||11–12-kb genome, polycistronic; Fig. 6; enveloped|
|VHSV, IHNV, HIRRV, SHRV, SVCV||Many fish species [e.g. Atlantic cod, coho salmon (Oncorhynchus kisutch), Pacific cod (Gadus macrocephalus), Pacific herring (Clupea pallasii)], penaeid shrimp||Serious impacts on aquaculture|
|DRV||White-beaked dolphin (Lagenorhynchus albirostris)||Possibly broad host range|
|Bunyaviridae||Three segments, 11–19-kb total genome; enveloped|
|Avalon, Farallon, Zaliv Terpeniya||Common murre, thick-billed murre, tufted puffin, Atlantic puffin (Fratercula arctica)||Transmission by invertebrate vectors at breeding colonies|
|13p2||American oyster (Crassostrea virginica)||11 segments, c. 24-kb total genome|
|CSRV||Chum salmon (Oncorhynchus keta)||11 segments, c. 24-kb total genome|
|P||Mediterranean swimming crab (Macropius depurator)||12 segments, c. 23-kb total genome|
|W2||Mediterranean shore crab (Carcinus mediterraneus)||12 segments, c. 24-kb total genome|
|MCRV||Mud crab (Scylla serrata)||13 segments, 26.9-kb total genome|
|MpRV||Micromonas pusilla (protist)||11 segments, 25.6-kb total genome|
|Bauline virus, Kemerovo virus, Okhotskiy virus||Common murre, thick-billed murre, tufted puffin, Atlantic puffin, razorbill (Alca torda)||Species Great Island virus|
Transmission by invertebrate vectors at breeding colonies
|IPNV||Many fish species [e.g. Atlantic salmon, red sea bream (Pagrus major), American plaice (Hippoglossoides platessoides), Atlantic cod], mollusks [e.g. Japanese pearl oyster (Pinctada fucata), jackknife clam (Sinonovacura constricta)]||3.1 and 2.7-kb bi-segmented genome; Fig. 6|
Widely distributed with serious impacts on aquaculture
|RV lemon shark||Lemon shark (Negaprion brevirostis)||Sequences amplified by PCR from fish genome|
|RV puffer fish||Puffer fish (Fugu rubripes)||Sequences amplified by PCR from fish genome|
|IMNV||Penaeid shrimp||7.6-kb genome; Fig. 6|
Most closely related to family Totiviridae
High mortalities in farmed shrimp