Viral-Mediated Microbe Mortality Modulated by Ocean Acidification and Eutrophication: Consequences for the Carbon Fluxes Through the Microbial Food Web.

Anthropogenic carbon emissions are causing changes in seawater carbonate chemistry including a decline in the pH of the oceans. While its aftermath for calcifying microbes has been widely studied, the effect of ocean acidification (OA) on marine viruses and their microbial hosts is controversial, and even more in combination with another anthropogenic stressor, i.e., human-induced nutrient loads. In this study, two mesocosm acidification experiments with Mediterranean waters from different seasons revealed distinct effects of OA on viruses and viral-mediated prokaryotic mortality depending on the trophic state and the successional stage of the plankton community. In the winter bloom situation, low fluorescence viruses, the most abundant virus-like particle (VLP) subpopulation comprising mostly bacteriophages, were negatively affected by lowered pH with nutrient addition, while the bacterial host abundance was stimulated. High fluorescence viruses, containing cyanophages, were stimulated by OA regardless of the nutrient conditions, while cyanobacteria of the genus Synechococcus were negatively affected by OA. Moreover, the abundance of very high fluorescence viruses infecting small haptophytes tended to be lower under acidification while their putative hosts' abundance was enhanced, suggesting a direct and negative effect of OA on viral-host interactions. In the oligotrophic summer situation, we found a stimulating effect of OA on total viral abundance and the viral populations, suggesting a cascading effect of the elevated pCO2 stimulating autotrophic and heterotrophic production. In winter, viral lysis accounted for 30 ± 16% of the loss of bacterial standing stock per day (VMMBSS) under increased pCO2 compared to 53 ± 35% in the control treatments, without effects of nutrient additions while in summer, OA had no significant effects on VMMBSS (35 ± 20% and 38 ± 5% per day in the OA and control treatments, respectively). We found that phage production and resulting organic carbon release rates significantly reduced under OA in the nutrient replete winter situation, but it was also observed that high nutrient loads lowered the negative effect of OA on viral lysis, suggesting an antagonistic interplay between these two major global ocean stressors in the Anthropocene. In summer, however, viral-mediated carbon release rates were lower and not affected by lowered pH. Eutrophication consistently stimulated viral production regardless of the season or initial conditions. Given the relevant role of viruses for marine carbon cycling and the biological carbon pump, these two anthropogenic stressors may modulate carbon fluxes through their effect on viruses at the base of the pelagic food web in a future global change scenario.

Enhanced Viral Activity in the Surface Microlayer of the Arctic and Antarctic Oceans.

The ocean surface microlayer (SML), with physicochemical characteristics different from those of subsurface waters (SSW), results in dense and active viral and microbial communities that may favor virus-host interactions. Conversely, wind speed and/or UV radiation could adversely affect virus infection. Furthermore, in polar regions, organic and inorganic nutrient inputs from melting ice may increase microbial activity in the SML. Since the role of viruses in the microbial food web of the SML is poorly understood in polar oceans, we aimed to study the impact of viruses on prokaryotic communities in the SML and in the SSW in Arctic and Antarctic waters. We hypothesized that a higher viral activity in the SML than in the SSW in both polar systems would be observed. We measured viral and prokaryote abundances, virus-mediated mortality on prokaryotes, heterotrophic and phototrophic nanoflagellate abundance, and environmental factors. In both polar zones, we found small differences in environmental factors between the SML and the SSW. In contrast, despite the adverse effect of wind, viral and prokaryote abundances and virus-mediated mortality on prokaryotes were higher in the SML than in the SSW. As a consequence, the higher carbon flux released by lysed cells in the SML than in the SSW would increase the pool of dissolved organic carbon (DOC) and be rapidly used by other prokaryotes to grow (the viral shunt). Thus, our results suggest that viral activity greatly contributes to the functioning of the microbial food web in the SML, which could influence the biogeochemical cycles of the water column.

Unveiling the role and life strategies of viruses from the surface to the dark ocean.

Viruses are a key component of marine ecosystems, but the assessment of their global role in regulating microbial communities and the flux of carbon is precluded by a paucity of data, particularly in the deep ocean. We assessed patterns in viral abundance and production and the role of viral lysis as a driver of prokaryote mortality, from surface to bathypelagic layers, across the tropical and subtropical oceans. Viral abundance showed significant differences between oceans in the epipelagic and mesopelagic, but not in the bathypelagic, and decreased with depth, with an average power-law scaling exponent of -1.03 km-1 from an average of 7.76 × 106 viruses ml-1 in the epipelagic to 0.62 × 106 viruses ml-1 in the bathypelagic layer with an average integrated (0 to 4000 m) viral stock of about 0.004 to 0.044 g C m-2, half of which is found below 775 m. Lysogenic viral production was higher than lytic viral production in surface waters, whereas the opposite was found in the bathypelagic, where prokaryotic mortality due to viruses was estimated to be 60 times higher than grazing. Free viruses had turnover times of 0.1 days in the bathypelagic, revealing that viruses in the bathypelagic are highly dynamic. On the basis of the rates of lysed prokaryotic cells, we estimated that viruses release 145 Gt C year-1 in the global tropical and subtropical oceans. The active viral processes reported here demonstrate the importance of viruses in the production of dissolved organic carbon in the dark ocean, a major pathway in carbon cycling.

Viruses and Protists Induced-mortality of Prokaryotes around the Antarctic Peninsula during the Austral Summer.

During the Austral summer 2009 we studied three areas surrounding the Antarctic Peninsula: the Bellingshausen Sea, the Bransfield Strait and the Weddell Sea. We aimed to investigate, whether viruses or protists were the main agents inducing prokaryotic mortality rates, and the sensitivity to temperature of prokaryotic heterotrophic production and mortality based on the activation energy (Ea) for each process. Seawater samples were taken at seven depths (0.1-100 m) to quantify viruses, prokaryotes and protists abundances, and heterotrophic prokaryotic production (PHP). Viral lytic production, lysogeny, and mortality rates of prokaryotes due to viruses and protists were estimated at surface (0.1-1 m) and at the Deep Fluorescence Maximum (DFM, 12-55 m) at eight representative stations of the three areas. The average viral lytic production ranged from 1.0 ± 0.3 × 107 viruses ml-1 d-1 in the Bellingshausen Sea to1.3 ± 0.7 × 107 viruses ml-1 d-1 in the Bransfield Strait, while lysogeny, when detectable, recorded the lowest value in the Bellingshausen Sea (0.05 ± 0.05 × 107 viruses ml-1 d-1) and the highest in the Weddell Sea (4.3 ± 3.5 × 107 viruses ml-1 d-1). Average mortality rates due to viruses ranged from 9.7 ± 6.1 × 104 cells ml-1 d-1 in the Weddell Sea to 14.3 ± 4.0 × 104 cells ml-1 d-1 in the Bellingshausen Sea, and were higher than averaged grazing rates in the Weddell Sea (5.9 ± 1.1 × 104 cells ml-1 d-1) and in the Bellingshausen Sea (6.8 ± 0.9 × 104 cells ml-1 d-1). The highest impact on prokaryotes by viruses and main differences between viral and protists activities were observed in surface samples: 17.8 ± 6.8 × 104 cells ml-1 d-1 and 6.5 ± 3.9 × 104 cells ml-1 d-1 in the Weddell Sea; 22.1 ± 9.6 × 104 cells ml-1 d-1 and 11.6 ± 1.4 × 104 cells ml-1 d-1 in the Bransfield Strait; and 16.1 ± 5.7 × 104 cells ml-1 d-1 and 7.9 ± 2.6 × 104 cells ml-1 d-1 in the Bellingshausen Sea, respectively. Furthermore, the rate of lysed cells and PHP showed higher sensitivity to temperature than grazing rates by protists. We conclude that viruses were more important mortality agents than protists mainly in surface waters and that viral activity has a higher sensitivity to temperature than grazing rates. This suggests a reduction of the carbon transferred through the microbial food-web that could have implications in the biogeochemical cycles in a future warmer ocean scenario.

Annual changes of bacterial mortality due to viruses and protists in an oligotrophic coastal environment (NW Mediterranean).

The impact of viruses and protists on bacterioplankton mortality was examined monthly during 2 years (May 2005-April 2007) in an oligotrophic coastal environment (NW Mediterranean Sea). We expected that in such type of system, (i) bacterial losses would be caused mainly by protists, and (ii) lysogeny would be an important type of virus-host interaction. During the study period, viruses and grazers together were responsible for 50.6 +/- 40.1% day(-1) of bacterial standing stock losses (BSS) and 59.7 +/- 44.0% day(-1) of bacterial production losses (BP). Over the first year (May 2005-April 2006), protists were the principal cause of bacterial mortality, removing 29.9 +/- 20.4% day(-1) of BSS and 33.9 +/- 24.3% day(-1) of BP, whereas viral lysis removed 13.5 +/- 17.0% day(-1) of BSS and 12.3 +/- 12.3% day(-1) of BP. During the second year (May 2006-April 2007), viruses caused comparable bacterial losses (29.2 +/- 14.8% day(-1) of BSS and 40.9 +/- 20.7% day(-1) of BP) to protists (28.6 +/- 25.5% day(-1) of BSS and 32.4 +/- 20.0% day(-1) of BP). In 37% of cases higher losses of BP due to viruses than due to protists were found. Lysogenic infection was detected in 11 of 24 samplings. Contrary to our expectations, lytic infections dominated over the two years, and viruses resulted to be a significant source of bacterial mortality in this oligotrophic site.