Abstract
ABSTRACTThe bloom-forming, toxic cyanobacterium Microcystis synthesizes multiple secondary metabolites and has been shown to deter zooplankton grazing. However, the biochemical and/or molecular basis by which Microcystis deters zooplankton remains unclear. This global transcriptomic study explored the response of Microcystis to direct and indirect exposures to multiple densities of two cladoceran grazers, Daphnia pulex and D. magna. Higher densities of both daphnids significantly reduced Microcystis cell densities and elicited a stronger transcriptional response in Microcystis. While many putative grazer deterrence genes (encoding microcystin, aeruginosin, cyanopeptolin, and microviridin) were largely unaffected by zooplankton, transcripts for heat shock proteins (hsp) increased in abundance. Beyond metabolites and hsp, large increases in the abundances of transcripts from photosynthetic processes were observed, evidencing energy acquisition pathways were stimulated by grazing. In addition, transcripts of genes associated with the production of extracellular polysaccharides and gas vesicles significantly increased in abundance. These genes have been associated with colony formation and may have been invoked to deter grazers. Collectively, this study demonstrates that daphnid grazers induce a significant transcriptomic response in Microcystis, suggesting this cyanobacterium upregulates specific biochemical pathways to adapt to predation.IMPORTANCE This work explores the transcriptomic responses of Microcystis aeruginosa following exposure to grazing by two cladocerans, Daphnia magna and D. pulex. Contrary to previous hypotheses, Microcystis did not employ putative grazing deterrent secondary metabolites in response to the cladocerans, suggesting they may have other roles within the cell, such as oxidative stress protection. The transcriptional metabolic signature during intense grazing was largely reflective of a growth and stress response, although increasing abundances of transcripts encoding extracellular polysaccharides and gas vesicles were potentially related to predator avoidance.
Highlights
The bloom-forming, toxic cyanobacterium Microcystis synthesizes multiple secondary metabolites and has been shown to deter zooplankton grazing
Microcystis cell densities were significantly reduced after 24 h of exposure to both Daphnia species at both daphnid densities relative to the control (Fig. 1A; one-way analysis of variance [ANOVA], P Ͻ0.05)
Microcystis Transcriptomic Grazing Response observed by the treatment with the largest number of D. magna (120 literϪ1), where the concentration of Microcystis cells was reduced by 80% (Fig. 1A)
Summary
The bloom-forming, toxic cyanobacterium Microcystis synthesizes multiple secondary metabolites and has been shown to deter zooplankton grazing. The biochemical and/or molecular basis by which Microcystis deters zooplankton remains unclear This global transcriptomic study explored the response of Microcystis to direct and indirect exposures to multiple densities of two cladoceran grazers, Daphnia pulex and D. magna. Higher densities of both daphnids significantly reduced Microcystis cell densities and elicited a stronger transcriptional response in Microcystis. Transcripts of genes associated with the production of extracellular polysaccharides and gas vesicles significantly increased in abundance These genes have been associated with colony formation and may have been invoked to deter grazers. Davis and Gobler [24] quantified grazing rates by multiple classes of zooplankton of microcystin- and nonmicrocystin-synthesizing strains of Microcystis in multiple ecosystems and found that microzooplankton and mesozooplankton grazed toxic and nontoxic strains with similar frequencies and rates
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