Sediments from Arctic Tide-Water Glaciers Remove Coastal Marine Viruses and Delay Host Infection.

Over the past few decades, the Arctic region has been strongly affected by global warming, leading to increased sea surface temperatures and melting of land and sea ice. Marine terminating (tide-water) glaciers are expected to show higher melting and calving rates, with an increase in the input of fine sediment particles in the coastal marine environment. We experimentally investigated whether marine viruses, which drive microbial interactions and biogeochemical cycling are removed from the water column through adsorption to glacier-delivered fine sediments. Ecologically relevant concentrations of 30, 100 and 200 mg·L-1 sediments were added to filtered lysates of 3 cultured algal viruses and to a natural marine bacterial virus community. Total virus removal increased with sediment concentration whereby the removal rate depended on the virus used (up to 88% for an Arctic algal virus), suggesting a different interaction strength with the sediment. Moreover, we observed that the adsorption of viruses to sediment is a reversible process, and that desorbed viruses are still able to infect their respective hosts. Nonetheless, the addition of sediment to infection experiments with the Arctic prasinovirus MpoV-45T substantially delayed host lysis and the production of progeny viruses. We demonstrate that glacier-derived fine sediments have the potency to alter virus availability and consequently, host population dynamics.

Influence of Irradiance and Temperature on the Virus MpoV-45T Infecting the Arctic Picophytoplankter Micromonas polaris.

Arctic marine ecosystems are currently undergoing rapid changes in temperature and light availability. Picophytoplankton, such as Micromonas polaris, are predicted to benefit from such changes. However, little is known about how these environmental changes affect the viruses that exert a strong mortality pressure on these small but omnipresent algae. Here we report on one-step infection experiments, combined with measurements of host physiology and viability, with 2 strains of M. polaris and the virus MpoV-45T under 3 light intensities (5, 60 and 160 µmol quanta m-2 s-1), 2 light period regimes (16:8 and 24:0 h light:dark cycle) and 2 temperatures (3 and 7 °C). Our results show that low light intensity (16:8 h light:dark) delayed the decline in photosynthetic efficiency and cell lysis, while decreasing burst size by 46%. In contrast, continuous light (24:0 h light:dark) shortened the latent period by 5 h for all light intensities, and even increased the maximum virus production rate and burst size under low light (by 157 and 69%, respectively). Higher temperature (7 °C vs 3 °C) led to earlier cell lysis and increased burst size (by 19%), except for the low light conditions. These findings demonstrate the ecological importance of light in combination with temperature as a controlling factor for Arctic phytoplankton host and virus dynamics seasonally, even more so in the light of global warming.

Characterization and Temperature Dependence of Arctic Micromonas polaris Viruses.

Global climate change-induced warming of the Artic seas is predicted to shift the phytoplankton community towards dominance of smaller-sized species due to global warming. Yet, little is known about their viral mortality agents despite the ecological importance of viruses regulating phytoplankton host dynamics and diversity. Here we report the isolation and basic characterization of four prasinoviruses infectious to the common Arctic picophytoplankter Micromonas. We furthermore assessed how temperature influenced viral infectivity and production. Phylogenetic analysis indicated that the putative double-stranded DNA (dsDNA) Micromonas polaris viruses (MpoVs) are prasinoviruses (Phycodnaviridae) of approximately 120 nm in particle size. One MpoV showed intrinsic differences to the other three viruses, i.e., larger genome size (205 ± 2 vs. 191 ± 3 Kb), broader host range, and longer latent period (39 vs. 18 h). Temperature increase shortened the latent periods (up to 50%), increased the burst size (up to 40%), and affected viral infectivity. However, the variability in response to temperature was high for the different viruses and host strains assessed, likely affecting the Arctic picoeukaryote community structure both in the short term (seasonal cycles) and long term (global warming).

Virus production in phosphorus-limited Micromonas pusilla stimulated by a supply of naturally low concentrations of different phosphorus sources, far into the lytic cycle.

Earlier studies show that the proliferation of phytoplankton viruses can be inhibited by depletion of soluble reactive phosphorus (SRP; orthophosphate). In natural marine waters, phytoplankton phosphorus (P) availability is, however, largely determined by the supply rate of SRP (e.g. through remineralization) and potentially by the source of P as well (i.e. the utilization of soluble non-reactive P; SNP). Here we show how a steady low supply of P (mimicking natural P recycling) to virally infected P-limited Micromonas pusilla stimulates virus proliferation. Independent of the degree of P limitation prior to infection (0.32 and 0.97µmax chemostat cultures), SRP supply resulted in 2-fold higher viral burst sizes (viruses lysed per host cell) as compared with no addition (P starvation). Delaying these spikes during the infection cycle showed that the added SRP was utilized for extra M. pusilla virus (MpV) production far into the lytic cycle (18 h post-infection). Moreover, P-limited M. pusilla utilized several SNP compounds with high efficiency and with the same extent of burst size stimulation as for SRP. Finally, addition of virus-free MpV lysate (representing a complex SNP mixture) to newly infected cells enhanced MpV production, implicating host-associated alkaline phosphatase activity, and highlighting its important role in oligotrophic environments.

Elevated CO2 and phosphate limitation favor Micromonas pusilla through stimulated growth and reduced viral impact.

Growth and viral infection of the marine picoeukaryote Micromonas pusilla was studied under a future-ocean scenario of elevated partial CO2 (pCO2; 750 µatm versus the present-day 370 µatm) and simultaneous limitation of phosphorus (P). Independent of the pCO2 level, the ratios of M. pusilla cellular carbon (C) to nitrogen (N), C:P and N:P, increased with increasing P stress. Furthermore, in the P-limited chemostats at growth rates of 0.32 and 0.97 of the maximum growth rate (µmax), the supply of elevated pCO2 led to an additional rise in cellular C:N and C:P ratios, as well as a 1.4-fold increase in M. pusilla abundance. Viral lysis was not affected by pCO2, but P limitation led to a 150% prolongation of the latent period (6 to 12 h) and an 80% reduction in viral burst sizes (63 viruses per cell) compared to P-replete conditions (4 to 8 h latent period and burst size of 320). Growth at 0.32 µmax further prolonged the latent period by another 150% (12 to 18 h). Thus, enhanced P stress due to climate change-induced strengthened vertical stratification can be expected to lead to reduced and delayed virus production in picoeukaryotes. This effect is tempered, but likely not counteracted, by the increase in cell abundance under elevated pCO2. Although the influence of potential P-limitation-relieving factors, such as the uptake of organic P and P utilization during infection, is unclear, our current results suggest that when P limitation prevails in future oceans, picoeukaryotes and grazing will be favored over larger-sized phytoplankton and viral lysis, with increased matter and nutrient flow to higher trophic levels.