Elevated CO ₂ and Phosphate Limitation Favor Micromonas pusilla through Stimulated Growth and Reduced Viral Impact

Abstract

bGrowth and viral infection of the marine picoeukaryote Micromonas pusilla was studied under a future-ocean scenario of elevated partial CO 2 (pCO 2 ; 750 atm versus the present-day 370 atm) and simultaneous limitation of phosphorus (P). Independent of the pCO 2 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 ( max ), the supply of elevated pCO 2 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 pCO 2 , 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 max 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 pCO 2 . 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.

The Arctic picoeukaryote <i>Micromonas</i> pusilla benefits synergistically from warming and ocean acidification

“…This finding is in line with previous studies, which have shown that picoeukaryotes can benefit 334 strongly from OA in both laboratory and mesocosm studies (Meakin and Wyman, 2011;335 Newbold et al, 2012;Schaum et al, 2012;Brussaard et al, 2013;Maat et al, 2014;Schulz et 336 al., 2017). Such positive response to OA could indicate that picoeukaryotes such as M. pusilla 337 are mainly dependent on diffusive CO 2 supply and thus directly benefit from higher CO 2 338 concentrations Schulz et al, 2013;Schulz et al, 2017).…”

“…Hence, this species can be expected to thrive well under conditions 399 expected for the end of this century (Stocker, 2014), potentially increasing its ecological 400 relevance even further. Regarding the importance of the nutrient availability, laboratory 401 experiments found beneficial OA effects on M. pusilla primary production to persist also under 402 P limitation (Maat et al, 2014), while in a mesocosm community, OA-dependent increases in 403 M. pusilla abundances disappeared when the system ran into P and N co-limitation (Engel et 404 al., 2008). Thus, it remains to be seen how the combined effects of warming and OA manifest 405 under low nutrient conditions.…”

Bridging the Gap between Knowing and Modeling Viruses in Marine Systems—An Upcoming Frontier

“…The impact of viruses on phytoplankton communities is also related to P-availability as the shortage of this nutrient is assumed to decrease the percentage of lysed cells (Wilson et al, 1996;Monier et al, 2012;Maat et al, 2016a,b). Recently, Maat et al (2014) have evaluated the outcome of P limitation on viral infection in picoeukaryote Micromonas pusilla, reporting a prolongation of the latent period from 6 to 12 h, and an 80% reduction in viral burst sizes compared to P-replete conditions. Phosphorus stress has been pointed out as a strong selective agent, with some phage having in their genome host-like phosphorus assimilation genes that are upregulated when the host is phosphorous starved, thus promoting P acquisition necessary for phage dispersion (Kelly et al, 2013).…”

Phytoplankton Virus Production Negatively Affected by Iron Limitation

“…Several studies using phytoplankton host-virus culture systems showed that major nutrient availability influences viral production and see review by Mojica and Brussaard, 2014). For example, phosphorus (P) limitation of the virally infected phytoplankton host results in a prolonged latent period, i.e., the time between infection and the initial release of progeny viruses from the host cell, for the infecting viruses (Maat et al, 2014). Moreover, P-stress resulted in reduced viral burst size, i.e., the number of newly formed viruses released per lysed host cell (Bratbak et al, 1998;Maat et al, 2014).…”

“…For example, phosphorus (P) limitation of the virally infected phytoplankton host results in a prolonged latent period, i.e., the time between infection and the initial release of progeny viruses from the host cell, for the infecting viruses (Maat et al, 2014). Moreover, P-stress resulted in reduced viral burst size, i.e., the number of newly formed viruses released per lysed host cell (Bratbak et al, 1998;Maat et al, 2014). These studies proposed shortage of phosphorus as a viral production substrate as well as possible host energy deficiency as reasons for the lower and delayed viral particle yield.…”