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Nitrogen and phosphorus significantly alter growth, nitrogen fixation, anatoxin-a content, and the transcriptome of the bloom-forming cyanobacterium, Dolichospermum.

ABSTRACT: While freshwater cyanobacteria are traditionally thought to be limited by the availability of phosphorus (P), fixed nitrogen (N) supply can promote the growth and/or toxin production of some genera. This study characterizes how growth on N₂ (control), nitrate (NO₃ ^-), ammonium (NH₄ ⁺), and urea as well as P limitation altered the growth, toxin production, N₂ fixation, and gene expression of an anatoxin-a (ATX-A) - producing strain of Dolichospermum sp. 54. The transcriptomes of fixed N and P-limited cultures differed significantly from those of fixed N-deplete, P-replete (control) cultures, while the transcriptomes of P-replete cultures amended with either NH₄ ⁺ or NO₃ ^- were not significantly different relative to those of the control. Growth rates of Dolichospermum (sp. 54) were significantly higher when grown on fixed N relative to without fixed N; growth on NH₄ ⁺ was also significantly greater than growth on NO₃ ^-. NH₄ ⁺ and urea significantly lowered N₂ fixation and nifD gene transcript abundance relative to the control while cultures amended with NO₃ ^- exhibited N₂ fixation and nifD gene transcript abundance that was not different from the control. Cultures grown on NH₄ ⁺ exhibited the lowest ATX-A content per cell and lower transcript abundance of genes associated ATX-A synthesis (ana), while the abundance of transcripts of several ana genes were highest under fixed N and P - limited conditions. The significant negative correlation between growth rate and cellular anatoxin quota as well as the significantly higher number of transcripts of ana genes in cultures deprived of fixed N and P relative to P-replete cultures amended with NH₄ ⁺ suggests ATX-A was being actively synthesized under P limitation. Collectively, these findings indicate that management strategies that do not regulate fixed N loading will leave eutrophic water bodies vulnerable to more intense and toxic (due to increased biomass) blooms of Dolichospermum.

SUBMITTER: Kramer BJ

PROVIDER: S-EPMC9490380 | biostudies-literature | 2022

REPOSITORIES: biostudies-literature

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Nitrogen and phosphorus significantly alter growth, nitrogen fixation, anatoxin-a content, and the transcriptome of the bloom-forming cyanobacterium, Dolichospermum.

Kramer Benjamin J BJ Jankowiak Jennifer G JG Nanjappa Deepak D Harke Matthew J MJ Gobler Christopher J CJ

Frontiers in microbiology 20220907

While freshwater cyanobacteria are traditionally thought to be limited by the availability of phosphorus (P), fixed nitrogen (N) supply can promote the growth and/or toxin production of some genera. This study characterizes how growth on N2 (control), nitrate (NO3 -), ammonium (NH4 +), and urea as well as P limitation altered the growth, toxin production, N2 fixation, and gene expression of an anatoxin-a (ATX-A) - producing strain ...[more]

PMID: 36160233

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Project description: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.

Dataset Information

Nitrogen and phosphorus significantly alter growth, nitrogen fixation, anatoxin-a content, and the transcriptome of the bloom-forming cyanobacterium, Dolichospermum.

Publications

Nitrogen and phosphorus significantly alter growth, nitrogen fixation, anatoxin-a content, and the transcriptome of the bloom-forming cyanobacterium, <i>Dolichospermum</i>.

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