Virus-induced mortality of microbes has direct effects on ecosystem function. Lysis of microbes involves the release of organic carbon and other nutrients back into the environment. This redirection is known as the viral shunt [8
]. The viral shunt denotes the fact that cellular materials released as particular or dissolved organic material are not directly available for utilization by organisms from higher trophic levels (e.g. plankton and fish) (see ) but are primarily utilized by predominantly heterotrophic bacteria, although some efforts have shown nutrients released in this manner to be rapidly assimilated by eukaryotic plankton [38
Direct efforts to estimate the viral shunt are rare, with most indirectly determining virus turnover rates and from this inferring virus-mediated elemental release. While several approaches exist to estimate virus production [39
], currently favoured approaches all depend on the same steps: dilution of samples and estimates of virus reoccurrence [31
]. Application of these approaches in recent years has begun to provide a broad overview of the variability of virus effects across different oceanic realms [40
], with all observations pointing to differing constraints on virus activities in different systems.
In addition, recent evidence suggests that viral lysis of microbes changes the relative distribution of dissolved organic matter with many indirect effects in ocean ecosystems. For example, viral lysis of microbes shifts organic matter from cells into dissolved and particular organic pools. The type of organic material released in viral lysis includes a spectrum of molecules ranging from bio-available (i.e. “labile”) to recalcitrant (see ) and may be dependent as much on the location of the lytic event as the players involved [44
]. In the deep ocean, the fate of virus-released organic matter remains a mystery, but this process may drive the generation of the ancient organic carbon measured by marine chemists [45
]. Moreover, it is known that virus activity may drive the formation of marine snow by releasing “sticky” components from within cells [46
], while at the same time disaggregating particles through cell lysis [44
]. Overall, we still know little about how virus activity changes the character of dissolved organic matter, the effect of viruses on carbon distribution (i.e. fixation, respiration, mineralization and export) in marine systems, despite the potential impacts on global budgets on both short-term and geological time scales.
Schematic of the role of viruses in the differential regeneration of organic matter
In addition to direct effects, the differential conversion of cellular material by viruses into a spectrum of dissolved organic material may indirectly
affect the growth of microbial populations. An intriguing hypothesis is that heterotrophs and autotrophs may be “primed” (i.e. stimulated) by the lysis of microbes [38
]. This includes the release of lysis byproducts that may stimulate the growth of a subset of heterotrophs [3
] as well as eukaryotic auxotrophs [52
]. Characterizing priming and its consequences constitutes an important area of future research, as determining the fate of carbon released from lysed cells is critical to understand how it is recycled or removed (i.e. rendered recalcitrant) from marine carbon budgets [44
]. The study of nutrients may also be critical to this goal, as it has been demonstrated that the release of bioavailable nutrient elements, including N and Fe [38
], may maintain ecosystem productivity under conditions where nutrient availability limits carbon production.
Finally, the infection of microbes also alters host metabolism, often in significant ways. For example, cyanophage-infecting cyanobacteria, such as Prochlorococcus sp.
and Synecochoccus sp.
, increase the overall photosynthetic rate of microbes, presumably changing the fixation rate of carbon from the environment before lysis. Cellular-based studies have confirmed that pathways within cells can be altered at the metabolic level [55
]. Similarly, persistent infections, such as occurs during lysogeny, can change the rate and type of utilization processes. Hence, infection can alter the behaviour of microbes, as seen from an ecosystem perspective. The net effect of such differential metabolism at the ecosystem level, however, remains largely unknown. Estimates of the contribution of lysogeny production to virus activity in marine systems remain highly variable [21
]. Future work should likely consider changes in cellular biochemistry as well as differences in cellular processes (e.g. growth efficiency, respiration and photosynthesis, etc.) between lysogens and uninfected cells. Quantifying these differences is likely to be an important component of efforts to census the overall rates at which viruses affect ecosystem functions.