VIRUSES IN AQUATIC ECOSYSTEMS - A REVIEW

Even though the contribution of water ecosystems for disseminating ent eric viral pathogens has been known for decades, the importance of wil d virions iii structuring aquatic communities and food webs has only c ome to light relatively recently. Evidences of viral infections in bot h pro-and eukaryotic phytoplankton, as well as in heterotrophic bacter io-and protozooplankton, have recently brought marine biologists to qu estion the impact of viroplankton on processes such as (1) the mortali ty of microorganisms, (2) the nutrition of heterotrophic protists, (3) the promotion of genetic material exchanges among microbial populatio ns, (4) the maintenance of species diversity, (5) the induction of pla nktonic aggregates, and (6) the cycling of organic matter in aquatic e cosystems. In this paper, all these points are reviewed and discussed, in the light of recent contributions to the ecology of aquatic viruse s, for evidence of the impact of viruses on both steady and non-steady state processes in fresh- and salt-waters. Viruses are ubiquitous, ab undant and dynamic components of pelagic ecosystems. They are, undoubt edly, more diversified than the phage-like morphotypes that are genera lly characterized by the presence of an icosa- or octahedral head and a tail, via observations under electron microscope. The diversity of p lanktonic viruses is further enhanced from the genetic viewpoint, and likely implies the diversity of sensible hosts. Genetically related ma rine phages are likely widely distributed in the space (i. e. without significant geographical segregation), suggesting prevalence of a redu ced competition among viral ''populations'', and that the main biotic limiting factor for a viral ''species'' production is the density of t he sensible host. Some viral ''species'', known from marine systems, t ypically harbor knob-like projections and long spines (i. e. previousl y not noted from non.-aquatic habitats), which are suggested to increa se the efficiency of hitting a specific host, especially in oligotroph ic waters. Despite the general scarcity of viral isolates that lyse ci liated protozooplankton and metazoan zooplankton, it is becoming incre asingly evident that most of the pelagic pro-and eukaryotic organisms are subject to infectious attacks from ambient ''free-living'' viruses . Quantitatively, recent total counts from the plankton generally fall in between 10(4) and 10(8) viruses ml(-1), with seasonal high densiti es in spring and summer, and a lowering tendency in abundance from the coastal to the open marine systems, and from the surface to the depth waters, likely in relation to temperature and the organic matter load . it was recently shown that lytic infection, rather than induction of lysogeny, is responsible for the majority of bacteriophage production in the plankton, especially in the coastal marine and surface waters and during blooming events, where the threshold-product level of virus x bacteria numbers of greater than or equal to 10(12) for the start o f a viral-lytic activity is generally achieved. Closed linear relation ships have been reported between viroplankton dynamics and bacteria, a lgae and nutrients. Because of the preponderance of allochtonous organ ic matter and cyanobacterial cells in lakes as compared to oceanic sys tems, the virus-to-bacteria ratio in lakes are significantly higher th an in marines systems, although there is little trend in the virus-to- bacteria ratio with increasing trophy, and despite the occurrence of m ore bacteria per unit chlorophyll in lake samples. The functional impa ct of virions on the structure and metabolism of planktonic communitie s is more important than their quantitative importance, as viruses rep resent only a minor fraction of the total planktonic biomass. The vira l-induced mortality of microbial communities in marine systems is esti mated to represent about 30 and < 10 pour 100 of the mortality of bact erio- and phytoplankton, respectively. Based on one study, the contrib ution of viruses to bacterial mortality in lakes seems considerably lo wer than in marine systems. The greatest impact of viruses on aquatic communities is likely through hazardous (i.e. non-steady state) proces ses which are difficult to quantified, such as the promotion of geneti c material exchanges among populations and the maintenance of species diversity. The lytic pressure from virulent viruses may act as a ''non stop'' inductor of modifications in the genetic heritage of host-organ isms, thereby increasing the potential of these hosts to share their h abitat with homologous species, i.e. with similar nutritional requirem ents. It has recently been shown that lysates resulting from phage inf ection can caused a significant increase in metabolic activity of noni nfected bacterioplankton community, but the growth efficiency of these noninfected hosts decreased in the presence of viruses, likely becaus e of the increase in bacterial energy demand associated with extracell ular degradation of polymers that are prevalent in viral lysates. This seems to verify the hypothesis on a substantial contribution of the l ytic activity from viruses, to the cycling of organic matter in aquati c systems. Viral lytic production may indeed (1) reduce the bacterial biomass contribution to the transfer of metabolic energy on to higher- order consumers, (2) result in an increase of bacterial secondary prod uction in the absence of an increase in the ambient primary production , and (3) increase competition between bacterial exo- or ectoenzyme ac tivity and the feeding activity of protozoa on high molecular weight p olymers (including viruses), although ingestion of viruses by protists seems to be of less importance in the carbon flows through the microb ial food web in pelagic systems. However, almost all studies on the ec ology of pelagic viruses are done during a limited period of year, mai nly in marine waters situated in temperate zones. The data discussed i n this paper are thus to be considered as preliminary data. Neverthele ss, viruses undoubtedly influence to various degrees the biological pr ocesses in aquatic ecosystems. The quantitative assessment of their fu nctional impact is thus required for incorporation into models that si mulate flues of matter, nutrients and energy in aquatic systems. This task is to be include on the agenda of both marine and freshwater biol ogists, as a high priority concern for the near future.