Algal viruses are important contributors to carbon cycling, recycling nutrients and organic material through host lysis. Although viral infection has been described as a primary mechanism of phytoplankton mortality, little is known about host defense responses. We show that viral infection of the bloom‐forming, planktonic diatom Although viral RNA was detected within spores, mature virions were not observed. ‘Infected’ spores were capable of germinating, but did not propagate or transmit infectious viruses. These results demonstrate that diatom spore formation is an effective defense strategy against viral‐mediated mortality. They provide a possible mechanistic link between viral infection, bloom termination, and mass carbon export events and highlight an unappreciated role of viruses in regulating diatom life cycle transitions and ecological success.
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Ecophysiological stress and the grazing of diatoms are known to elicit the production of chemical defense compounds called oxylipins, which are toxic to a wide range of marine organisms. Here we show that (1) the viral infection and lysis of diatoms resulted in oxylipin production; (2) the suite of compounds produced depended on the diatom host and the infecting virus; and (3) the virus-mediated oxylipidome was distinct, in both magnitude and diversity, from oxylipins produced due to stress associated with the growth phase. We used high-resolution accurate-mass mass spectrometry to observe changes in the dissolved lipidome of diatom cells infected with viruses over 3 to 4 days, compared to diatom cells in exponential, stationary, and decline phases of growth. Three host virus pairs were used as model systems: Chaetoceros tenuissimus infected with CtenDNAV; C. tenuissimus infected with CtenRNAV; and Chaetoceros socialis infected with CsfrRNAV. Several of the compounds that were significantly overproduced during viral infection are known to decrease the reproductive success of copepods and interfere with microzooplankton grazing. Specifically, oxylipins associated with allelopathy towards zooplankton from the 6-, 9-, 11-, and 15-lipogenase (LOX) pathways were significantly more abundant during viral lysis. 9-hydroperoxy hexadecatetraenoic acid was identified as the strongest biomarker for the infection of Chaetoceros diatoms. C. tenuissimus produced longer, more oxidized oxylipins when lysed by CtenRNAV compared to CtenDNAV. However, CtenDNAV caused a more statistically significant response in the lipidome, producing more oxylipins from known diatom LOX pathways than CtenRNAV. A smaller set of compounds was significantly more abundant in stationary and declining C. tenuissimus and C. socialis controls. Two allelopathic oxylipins in the 15-LOX pathway and essential fatty acids, arachidonic acid (ARA), eicosapentaenoic acid (EPA), and docosahexaenoic acid (DHA) were more abundant in the stationary phase than during the lysis of C. socialis. The host–virus pair comparisons underscore the species-level differences in oxylipin production and the value of screening more host–virus systems. We propose that the viral infection of diatoms elicits chemical defense via oxylipins which deters grazing with downstream trophic and biogeochemical effects.
more » « less- PAR ID:
- 10508262
- Editor(s):
- Lauritano, Chiara; Ianora, Adrianna
- Publisher / Repository:
- MDPI
- Date Published:
- Journal Name:
- Marine Drugs
- Volume:
- 22
- Issue:
- 5
- ISSN:
- 1660-3397
- Page Range / eLocation ID:
- 228
- Subject(s) / Keyword(s):
- oxylipins chemical signaling lipidomics diatom viruses marine virology allelopathy viral ecology lipid dissolved organic matter orbitrap mass spectrometry
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Summary Chaetoceros socialis induces the mass formation of resting spores, a heavily silicified life cycle stage associated with carbon export due to rapid sinking. -
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