Nitric oxide production and antioxidant function during viral infection of the coccolithophore Emiliania huxleyi

Abstract

Emiliania huxleyi is a globally important marine phytoplankton that is routinely infected by viruses. Understanding the controls on the growth and demise of E. huxleyi blooms is essential for predicting the biogeochemical fate of their organic carbon and nutrients. In this study, we show that the production of nitric oxide (NO), a gaseous, membrane-permeable free radical, is a hallmark of early-stage lytic infection in E. huxleyi by Coccolithoviruses, both in culture and in natural populations in the North Atlantic. Enhanced NO production was detected both intra- and extra-cellularly in laboratory cultures, and treatment of cells with an NO scavenger significantly reduced viral production. Pre-treatment of exponentially growing E. huxleyi cultures with the NO donor S-nitroso-N-acetylpenicillamine (SNAP) prior to challenge with hydrogen peroxide (H 2 O 2 ) led to greater cell survival, suggesting that NO may have a cellular antioxidant function. Indeed, cell lysates generated from cultures treated with SNAP and undergoing infection displayed enhanced ability to detoxify H 2 O 2 . Lastly, we show that fluorescent indicators of cellular ROS, NO, and death, in combination with classic DNA- and lipid-based biomarkers of infection, can function as real-time diagnostic tools to identify and contextualize viral infection in natural E. huxleyi blooms.

Viability of pico- and nanophytoplankton in the Baltic Sea during spring

“…Cell death is a third loss factor, but its quantification in marine systems, and aquatic systems in general, remains rare compared to the quantification of sinking and grazing losses. Phytoplankton cell death can be caused by pathogens (Bramucci and Case 2019;Schieler et al 2019) or physiological stress, and a handful of studies indicate that a considerable proportion of phytoplankton cells may not be viable (e.g. Brussaard et al 1995;Veldhuis et al 2001;Agustí 2004;Berman-Frank et al 2004;Rychtecký et al 2014).…”

Temperate infection in a virus–host system previously known for virulent dynamics

“…The E. huxleyi-EhV system is a fundamental model of virulent infection dynamics. Infection in high-density lab cultures and nutrient-amended, eutrophic mesocosms (10 5 -10 6 cells per milliliter; "crowded" densities) result in host death and bloom termination within days 25,31,[37][38][39] . In stark contrast, natural E. huxleyi bloom densities across the global ocean are almost exclusively 10 3 cells per milliliter or less (hereafter referred to as "sparse" densities; Fig.…”

“…However, they are indistinguishable at the host densities of ≥10 5 cells per milliliter that are commonly used in laboratory and mesocosm experiments (Fig. 3e) 25,27,31,35,38 because temperate viruses rapidly initiate lysis when hosts become stressed at these high densities. Under these conditions, the viruses act as if they are virulent despite having the capacity to be temperate.…”

Promises and Challenges of Microalgal Antioxidant Production

“…These results point to the reason that there is such great interest in the highly promising microalgae as antioxidant providers for nutraceuticals and human wellness, and invoke the necessity of further exploring this great potential. The relevant antioxidant activity is probably related to the high content and diversity of antioxidant molecules in microalgae, which are a source of a wide range of antioxidant molecules [42,43,44,45,46,47,48] (Figure 1), some of which are aquatic-specific, while others are shared with terrestrial plants.…”