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Influence of cyanobacteria, mixotrophic flagellates, and virioplankton size fraction on transcription of microcystin synthesis genes in the toxic cyanobacterium Microcystis aeruginosa.

ABSTRACT: Toxic cyanobacteria such as Microcystis aeruginosa are a worldwide concern in freshwater reservoirs. Problems associated with their mass occurrence are predicted to increase in the future due to global warming. The hepatotoxic secondary metabolite microcystin is of particular concern in this context. This study aimed to determine whether co-occurring microorganisms influence the expression of microcystin biosynthesis genes. To this end, we performed cocultivation experiments and measured mcyB and mcyD transcripts in M. aeruginosa using RT-qPCR. We utilized representatives from three different plankton groups: the picocyanobacterium Synechococcus elongatus, the unicellular flagellate grazer Ochromonas danica, and virioplankton from two different lakes. The presence of S. elongatus significantly increased mcyB and mcyD transcription in M. aeruginosa. Cocultivation with the mixotrophic chrysophyte O. danica did not increase the transcription of mcyB and mcyD; in fact, mcyD transcripts decreased significantly. The virioplankton size fraction of environmental water samples induced a significant increase in mcyB and mcyD transcription when obtained from lakes with cyanobacterial blooms. Our results show that co-occurring microorganisms influence the expression of microcystin biosynthesis genes in M. aeruginosa.

SUBMITTER: Scherer PI

PROVIDER: S-EPMC5822348 | biostudies-literature | 2018 Feb

REPOSITORIES: biostudies-literature

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Influence of cyanobacteria, mixotrophic flagellates, and virioplankton size fraction on transcription of microcystin synthesis genes in the toxic cyanobacterium Microcystis aeruginosa.

Scherer Pia I PI Absmeier Carolin C Urban Maria M Raeder Uta U Geist Juergen J Zwirglmaier Katrin K

MicrobiologyOpen 20170925 1

Toxic cyanobacteria such as Microcystis aeruginosa are a worldwide concern in freshwater reservoirs. Problems associated with their mass occurrence are predicted to increase in the future due to global warming. The hepatotoxic secondary metabolite microcystin is of particular concern in this context. This study aimed to determine whether co-occurring microorganisms influence the expression of microcystin biosynthesis genes. To this end, we performed cocultivation experiments and measured mcyB an ...[more]

PMID: 28944994

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Project description:BackgroundThe water-bloom-forming cyanobacterium Microcystis aeruginosa is a known producer of various kinds of toxic and bioactive chemicals. Of these, hepatotoxic cyclic heptapeptides microcystins have been studied most intensively due to increasing concerns for human health risks and environmental damage. More than 70 variants of microcystins are known, and a single microcystin synthetase (mcy) gene cluster consisting of 10 genes (mcyA to mcyJ) has been identified to be responsible for the production of all known variants of microcystins. Our previous multilocus sequence typing (MLST) analysis of the seven housekeeping genes indicated that microcystin-producing strains of M. aeruginosa are classified into two phylogenetic groups.ResultsTo investigate whether the mcy genes are genetically structured similarly as in MLST analysis of the housekeeping genes and to identify the evolutionary forces responsible for the genetic divergence of these genes, we used 118 mcy-positive isolates to perform phylogenetic and population genetic analyses of mcy genes based on three mcy loci within the mcy gene cluster (mcyD, mcyG, and mcyJ), none of which is involved in the production of different microcystin variants. Both individual phylogenetic analysis and multilocus genealogical analysis of the mcy genes divided our isolates into two clades, consistent with the MLST phylogeny based on seven housekeeping loci. No shared characteristics within each clade are known, and microcystin analyses did not identify any compositional trend specific to each clade. Statistical analyses for recombination indicated that recombination among the mcy genes is much more frequent within clades than between, suggesting that recombination has been an important force maintaining the cryptic divergence of mcy genes. On the other hand, a series of statistical tests provided no strong evidence for selection to explain the deep divergence of the mcy genes. Furthermore, analysis of molecular variance (AMOVA) indicated a low level of geographic structuring in the genetic diversity of mcy.ConclusionOur phylogenetic analyses suggest that the mcy genes of M. aeruginosa are subdivided into two cryptic clades, consistent with the phylogeny determined by MLST. Population genetic analyses suggest that these two clades have primarily been maintained as a result of homology-dependent recombination and neutral genetic drift.

Project description:BACKGROUND:While transcriptomics have become a valuable tool for linking physiology and ecology in aquatic microbes, the temporal dynamics of global transcriptomic patterns in Microcystis have rarely been assessed. Furthermore, while many microbial studies have explored expression of nutrient transporter genes, few studies have concurrently measured nutrient assimilation rates. Here, we considered how the global transcriptomic patterns and physiology of the cyanobacterium, Microcystis aeruginosa, changed daily as cells were grown from replete to deficient nitrogen (N) conditions and then back to replete conditions. RESULTS:During N deprivation, Microcystis downregulated genes involved in photosynthesis and respiration, carbon acquisition, lipid metabolism, and amino acid biosynthesis while upregulating genes involved in N acquisition and transport. With increasing N stress, both the strength of expression and number of genes being differentially expressed increased, until N was restored at which point these patterns reversed. Uptake of (15)N-labeled nitrate, ammonium and urea reflected differential expression of genes encoding transporters for these nutrients, with Microcystis appearing to preferentially increase transcription of ammonium and urea transporters and uptake of these compounds during N deprivation. Nitrate uptake and nitrate transporter expression were correlated for one set of transporters but not another, indicating these were high and low affinity nitrate transporters, respectively. Concentrations of microcystin per cell decreased during N deprivation and increased upon N restoration. However, the transcript abundance of genes involved in the synthesis of this compound was complex, as microcystin synthetase genes involved in peptide synthesis were downregulated under N deprivation while genes involved in tailoring and transport were upregulated, suggesting modification of the microcystin molecule under N stress as well as potential alternative functions for these genes and/or this toxin. CONCLUSIONS:Collectively, this study highlights the complex choreography of gene expression, cell physiology, and toxin synthesis that dynamic N levels can elicit in this ecologically important cyanobacterium. Differing expression patterns of genes within the microcystin synthetase operon in response to changing N levels revealed the potential limitations drawing conclusions based on only one gene in this operon.

Dataset Information

Influence of cyanobacteria, mixotrophic flagellates, and virioplankton size fraction on transcription of microcystin synthesis genes in the toxic cyanobacterium Microcystis aeruginosa.

Publications

Influence of cyanobacteria, mixotrophic flagellates, and virioplankton size fraction on transcription of microcystin synthesis genes in the toxic cyanobacterium Microcystis aeruginosa.

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