Abstract

Extracellular vesicles are produced by organisms from all kingdoms and serve a myriad of functions, many of which involve cell-cell signaling, especially during stress conditions and host-pathogen interactions. In the marine environment, communication between microorganisms can shape trophic level interactions and population succession, yet we know very little about the involvement of vesicles in these processes. In a previous study, we showed that vesicles produced during viral infection by the ecologically important model alga Emiliania huxleyi, could act as a pro-viral signal, by expediting infection and enhancing the half-life of the virus in the extracellular milieu. Here, we expand our laboratory findings and show the effect of vesicles on natural populations of E. huxleyi in a mesocosm setting. We profile the small-RNA (sRNA) cargo of vesicles that were produced by E. huxleyi during bloom succession, and show that vesicles applied to natural assemblages expedite viral infection and prolong the half-life of this major mortality agent of E. huxleyi. We subsequently reveal that exposure of the natural assemblage to E. huxleyi-derived vesicles modulates not only host-virus dynamics, but also other components of the microbial food webs, thus emphasizing the importance of extracellular vesicles to microbial interactions in the marine environment.

Highlights

  • The eukaryotic phytoplankter Emiliania huxleyi is a major contributor to the marine ecosystem

  • We previously showed that cultured E. huxleyi increases the production of vesicles during viral infection

  • We suggest that extracellular vesicles expedite viral infection in E. huxleyi cultures and during bloom demise

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Summary

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The eukaryotic phytoplankter Emiliania huxleyi is a major contributor to the marine ecosystem. In vesicle samples from all time points, we detected sRNA sequences that potentially regulate the E. huxleyi gene comp17003623_c0, which encodes a putative cation transport protein (Table S1) These cargo molecules may change the ability of target E. huxleyi cells to transport organic molecules and, change their metabolic profile. Treatment of the natural population taken from E. huxleyi demise phase (day 20, Fig. 2b), when EhV was clearly present in the population (Fig. 1b), led to a significant reduction in the abundance of nanophytoplankton, a group that includes E. huxleyi This was accompanied by an elevated EhV-like particle abundance as compared to the control populations that were not exposed to vesicles (Fig. 2b). We propose that communication via extracellular vesicles during microbial interactions in algal blooms may have a profound effect on the growth and composition of the associated marine microbial food webs

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