Transcriptomic Responses in the Bloom-Forming Cyanobacterium Microcystis Induced during Exposure to Zooplankton

Abstract

The 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.

Chemically mediated interactions between Microcystis and Planktothrix: impact on their growth, morphology and metabolic profiles

“…Simultaneously, transcriptome‐based characterization of interactions between co‐occurring organisms would contribute to the current knowledge about the molecular mechanisms involved in the intraspecies and interspecies cyanobacterial interactions. Regulatory molecular mechanisms, such as activity of transposable elements, enabling cells to face various environmental conditions, like N availability (Steffen et al ., ) and grazing (Harke et al ., ), may facilitate adaptability through the regulation of the production of metabolites.…”

“…Simultaneously, transcriptome-based characterization of interactions between co-occurring organisms would contribute to the current knowledge about the molecular mechanisms involved in the intraspecies and interspecies cyanobacterial interactions. Regulatory molecular mechanisms, such as activity of transposable elements, enabling cells to face various environmental conditions, like N availability (Steffen et al, 2014) and grazing (Harke et al, 2017), may facilitate adaptability through the regulation of the production of metabolites. Despite being conducted under laboratory conditions and on two species belonging to two genera, our experiments provide evidence that chemical cue(s) specific to each strain induced the stimulated production of intracellular compounds and the negative impact on Planktothrix growth, supporting the idea that cyanobacteria have the potential to interact with each other via released compounds.…”

High Diversity of Microcystin Chemotypes within a Summer Bloom of the Cyanobacterium Microcystis botrys

“…However, the evolution of microcystin synthetase genes pre-dates the occurrence of metazoans [32]. In fact, a transcriptome study showed that genes coding for putative grazer deterring compounds (such as microcystin), were largely unaffected when Microcystis was exposed to predators [61]. On the other hand, field studies have shown that microcystin concentrations are correlated to zooplankton composition, where high concentrations appear detrimental to potential grazers [49,62].…”

Molecular prediction of lytic vs lysogenic states for Microcystis phage: Metatranscriptomic evidence of lysogeny during large bloom events

“…Recent impacts include the shutdown of the public water supply to the City of Toledo (Ohio) during the Microcystis bloom in 2014 [ 11 ], and the considerable accumulation of toxic algal biomass in Lake Tai, China ( Taihu in Chinese) [ 12 , 13 ]. While significant strides have been made describing the ecology [ 14 – 16 ], physiology [ 17 – 19 ], and genetics [ 20 – 22 ] of Microcystis , little is known about the effect of phage on Microcystis ecology. To date, only 11 viruses infecting M .…”