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Viruses Systems in Marine Planktonic FEATURE VIRUSES IN MARINE PLANKTONIC SYSTEMS By Jed A. Fuhrman and Curtis A. Suttle Introduction ing regular structures such as icosahedrons (with The last 10-15 years have seen major changes or without a "tail"), filaments, and types with vari- in our views of marine planktonic food webs, pri- able morphology types (Figs. 1 and 2). marily from the realization that prokaryotic mi- There are three basic viral life cycles, all of croorganisms and small eukaryotes are responsible which start with attachment of the virus to a for a significant fraction, often 50% or more, of specific site and injection of the viral nucleic acid the primary production and heterotrophic con- into the host cell (Fig. 3). In the lytic cycle, this sumption of organic matter in these systems nucleic acid "'commands" the cell to produce mul- (Williams, 1981: Azam et al., 1983: Stockner and tiple viral progeny (often tens to hundreds) that Antia, 1986: Fuhrman, 1992). However, it has are released into the environment when the host only been in the past few years that marine scien- cell lyses (bursts). Also common among prokary- tists have investigated the roles of viruses in eco- otes is a process called lysogeny, in which the in- • . early results sug- logical processes. Although this research area is jected nucleic acid can become integrated into the only in its infancy, early results suggest that host's genome. This "provirus'" is reproduced gest that viruses may viruses may be important agents in the mortality along with the host DNA for many generations of marine microorganisms and in controlling their until the survival of the host is threatened, at be important agents in genetic compositions. This paper will summarize which time specific biochemical mechanisms can the mortality of marine the experiments and measurements that have led trigger the onset of the lytic cycle. Viruses capable to this suggestion as well as the conceptual frame- of lysogeny are called "'temperate," and they can microorganisms . work within which they are interpreted. be lysogenic in certain strains of hosts, and purely Viruses are fundamentally different from most lytic in others. Many bacterial isolates have been other biological entities in that they have no me- found to be lysogens, which means that they har- tabolism of their own and must rely on a host or- bor one or more proviruses that can be induced to ganism for any energy-requiring process, includ- become lytic. Among both prokaryotes and eu- ing reproduction. In many cases the host-virus karyotes, "chronic infections" can also occur relationship is very specific, with the viruses in- where viral progeny are produced and shed from fecting a single species or sometimes subspecies the host via budding or extrusion of filaments, or genus. Because most organisms seem to be sus- while host metabolism and reproduction proceed ceptible to viral infection, this suggests there are relatively unaltered. In metazoans viral infections millions of different kinds of viruses• They are are usually specific to certain tissues or organs. very small, usually from 20 to 250 nm in diameter The Presence and Abundance of Marine (hence they would be defined by most chemical Viruses oceanographers as "'dissolved organic matter"). They are composed of nucleic acid packaged in a Viruses it!fecting specific hosts protein coat, with some viruses having lipid pre- The existence of viruses in the marine environ- sent as well. The nucleic acid can be DNA or ment has been known for many years (e.g., Kriss RNA, either of which can be single- or double- and Rukina, 1947: Spencer, 1955, 1960), although stranded. There are several morphologies, includ- most of the early studies were concerned less with enumerating viruses than with characterizing iso- lates in terms of salinity and temperature effects, J.A. Fuhrman, Department of Biological Sciences, Univer- morphology, host range, etc. (e.g., Spencer, 1960: sity of Southern California, Los Angeles, CA 90089-0371, Hidaka, 1971: Hidaka and Fujimura, 1971; USA. C.A. Suttle, Marine Science Institute, The University of Texas at Austin, PO Box 1267, Port Aransas, TX 78373-1267, Zachary, 1976, 1978; Baross et al., 1978, see re- USA. view by BOrsheim, 1993). These studies focused OCEANO(;RAPH'~'Vo]. 6, No. 2°1993 5] polyhedral virus, 130-135 nm in diameter, that caused lysis of a widely distributed photosynthetic Head flagellate, Micromonas pusilla. They tested 35 dif- ferent species from five classes of algae and found that the virus was specific for M. pusilla. Despite the potential ecological significance of their obser- vations and indications that the virus could achieve high concentrations in seawater, research beyond initial characterization of the virus life cycle (Waters and Chan, 1982) was not pursued. It was not until more than a decade later that it was shown that viruses infecting representatives from a number of important groups of phytoplankton including cyanobacteria, diatoms, a prasinophyte, and a cryptophyte could be readily isolated from seawater (Suttle et al. 1990). Concentrations of viruses which infect particu- © lar hosts can vary widely, ranging from less than a few viruses per liter of seawater to concentrations > 108 L ~. For example, Spencer (1960) and Moe- bus (1987, 1992b) most often found abundances < 104 L-' for phages that infected marine bacterial Fig. 1: General morphologies of viruses (primarily bacteriophages), modified cultures. However, in the Kiel Bight (a somewhat from Ackermann and DuBow (1978). Another common term.for the head is polluted embayment of the Baltic Sea), Ahrens "capsid." Typical head diameters are 20-200 nm, although some larger ones (1971) found up to 3.7 X 107 phage L ~ that in- are known. Of the types shown, the only ones readily recognized in electron fected a strain of Agrobacterium stellatum, and micrographs from seawater are those with polyhedral heads (see Fig.2). Fila- Moebus (1992b) reported counts near Helgoland, mentous ones, which are ve~ flexible and are represented by the long thin rec- Germany, sometimes as high as 1.5 X 107 phage tangle on the right, and irregularly shaped ones are not easily distinguished L-' infecting one host strain; the highest abun- from other filaments or similar sized "blobs" in seawater. dances tended to last only a few days. In the coastal waters of Texas the concentration of phages that infect two taxonomically uncharacter- on viruses infecting bacteria (bacteriophages or ized marine bacteria (PWH3a and LMG1) varies phages). If such studies can be used as a guide, temporally and spatially, and is different for the the potential for viral infection seems high, as two hosts. For example, titers of viruses infecting 10-50% of marine bacteria isolates have been re- PWH3a varied from <0.7 to 101 L '; whereas, in ported to be susceptible to infection by cultured the same sample viruses infecting LMG1 ranged phage (Hidaka, 1977). However, Moebus and between 12 and 3.97 × 10 ~ L ~ (Suttle et al., Nattkemper (1983), who studied phage sensitivity 1991). The high densities were coincident with a of 1,382 bacterial isolates and found that many toxic dinoflagellate bloom. In the coral reef envi- could be infected with culturable phages, sug- ronment near Key Largo, Florida, bacteriophages gested that this might be because bacteria that can infecting cultured Vibrio species were also spa- be isolated from seawater may be particularly sus- tially variable, generally reaching highest concen- ceptible to such phages. trations (>75L -') in the nearshore and inshore envi- Evidence of viral infections in photosynthetic ronments where salinities were lowest (ca. 28-30 marine organisms began to accumulate in the ppt) and decreasing offshore where salinities were 1970s with a number of observations showing the >34 ppt (Paul et al., 1993). However, comparably The great variability of presence of virus-like particles (VLPs) in cultures high phage concentrations were found at one off- and natural assemblages of phytoplankton (e.g., shore station. Concentrations of viruses that infect specific virus abun- Chapman and Lang, 1973; Pienaar, 1976; see also photosynthetic plankton are also extremely vari- dances probably largely reviews by Dodds, 1979, 1983; Van Etten et al., able. For instance, viruses that infect the photo- 1991). These studies, however, provided no evi- synthetic flagellate Micromonas pusilla range in reflects the variability of dence that there were viruses in seawater that titer from <20 L' in the central Gulf of Mexico to host abundances... could infect and kill phytoplankton, although even 4.6 x 10~ L-' in some coastal water samples (Cot- earlier studies (e.g., Safferman and Morris, 1963, trell and Suttle, 1991). The great variability of 1967) had demonstrated the presence of viruses specific virus abundances probably largely reflects that infected freshwater cyanobacteria (prokaryotic the variability of host abundances, because the phytoplankton). The first evidence of infective viruses are dependent on hosts for reproduction. "phycoviruses" in seawater was provided by Of viruses infecting specific hosts, those found in Mayer and Taylor (1979) who isolated a large the highest known concentrations are cyanophages 52 OCEANOGRAPHY'VoI, 6, No. 2-1993 E Fig. 2: Transmission electron micrographs showing the morphological diversity of marine viruses. A-C), Natural virus communities from the Gulf of Mexico; D and F), Cyanophages (S-PWM4 & S-PWP1), which infect strains of Synechococcus spp., E) Virus (MPV-SP1), which
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