Closely related viruses of the marine picoeukaryotic alga Ostreococcus lucimarinus exhibit different ecological strategies

Zimmerman AE, Bachy C, Ma X, Roux S, Jang HB, Sullivan MB, Waldbauer JR, Worden AZ – Environmental Microbiology

In marine ecosystems, viruses are major disrupters of the direct flow of carbon and nutrients to higher trophic levels. Although the genetic diversity of several eukaryotic phytoplankton virus groups has been characterized, their infection dynamics are less understood, such that the physiological and ecological implications of their diversity remain unclear. We compared genomes and infection phenotypes of the two most closely related cultured phycodnaviruses infecting the widespread picoprasinophyte Ostreococcus lucimarinus under standard‐ (1.3 divisions per day) and limited‐light (0.41 divisions per day) nutrient replete conditions. OlV7 infection caused early arrest of the host cell cycle, coinciding with a significantly higher proportion of infected cells than OlV1‐amended treatments, regardless of host growth rate. OlV7 treatments showed a near‐50‐fold increase of progeny virions at the higher host growth rate, contrasting with OlV1’s 16‐fold increase. However, production of OlV7 virions was more sensitive than OlV1 production to reduced host growth rate, suggesting fitness trade‐offs between infection efficiency and resilience to host physiology. Moreover, although organic matter released from OlV1‐ and OlV7‐infected hosts had broadly similar chemical composition, some distinct molecular signatures were observed. Collectively, these results suggest that current views on viral relatedness through marker and core gene analyses underplay operational divergence and consequences for host ecology.

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Transcriptional responses of the marine green alga Micromonas pusilla and an infecting prasinovirus under different phosphate conditions

Prasinophytes are widespread marine algae for which responses to nutrient limitation and viral infection are not well understood. We studied the picoprasinophyte, Micromonas pusilla, grown under phosphate‐replete (0.65 ± 0.07 d−1) and 10‐fold lower (low)‐phosphate (0.11 ± 0.04 d−1) conditions, and infected by the phycodnavirus MpV‐SP1. Expression of 17% of Micromonas genes in uninfected cells differed by >1.5‐fold (q < 0.01) between nutrient conditions, with genes for P‐metabolism and the uniquely‐enriched Sel1‐like repeat (SLR) family having higher relative transcript abundances, while phospholipid‐synthesis genes were lower in low‐P than P‐replete. Approximately 70% (P‐replete) and 30% (low‐P) of cells were lysed 24 h post‐infection, and expression of ≤5.8% of host genes changed relative to uninfected treatments. Host genes for CAZymes and glycolysis were activated by infection, supporting importance in viral production, which was significantly lower in slower growing (low‐P) hosts. All MpV‐SP1 genes were expressed, and our analyses suggest responses to differing host‐phosphate backgrounds involve few viral genes, while the temporal program of infection involves many more, and is largely independent of host‐phosphate background. Our study (i) identifies genes previously unassociated with nutrient acclimation or viral infection, (ii) provides insights into the temporal program of prasinovirus gene expression by hosts and (iii) establishes cell biological aspects of an ecologically important host‐prasinovirus system that differ from other marine algal‐virus systems.

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