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Cooccurrence of Broad- and Narrow-Host-Range Viruses Infecting the Bloom-Forming Toxic Cyanobacterium Microcystis aeruginosa.

ABSTRACT: Viruses play important roles in regulating the abundance and composition of bacterial populations in aquatic ecosystems. The bloom-forming toxic cyanobacterium Microcystis aeruginosa is predicted to interact with diverse cyanoviruses, resulting in Microcystis population diversification. However, current knowledge of the genomes from these viruses and their infection programs is limited to those of Microcystis virus Ma-LMM01. Here, we performed a time series sampling at a small pond in Japan during a Microcystis bloom and then investigated the genomic information and transcriptional dynamics of Microcystis-interacting viruses using metagenomic and metatranscriptomic approaches. We identified 15 viral genomic fragments classified into three groups, groups I (including Ma-LMM01), II (high abundance and transcriptional activity), and III (new lineages). According to the phylogenetic distribution of Microcystis strains possessing spacers against each viral group, the group II-original viruses interacted with all three phylogenetically distinct Microcystis population types (phylotypes), whereas the groups I and III-original viruses interacted with only one or two phylotypes, indicating the cooccurrence of broad- (group II) and narrow (groups I and III)-host-range viruses in the bloom. These viral fragments showed the highest transcriptional levels during daytime regardless of their genomic differences. Interestingly, M. aeruginosa expressed antiviral defense genes in the environment, unlike what was seen with an Ma-LMM01 infection in a previous culture experiment. Given that broad-host-range viruses often induce antiviral responses within alternative hosts, our findings suggest that such antiviral responses might inhibit viral multiplication, mainly that of broad-host-range viruses like those in group II.IMPORTANCE The bloom-forming toxic cyanobacterium Microcystis aeruginosa is thought to have diversified its population through the interactions between host and viruses in antiviral defense systems. However, current knowledge of viral genomes and infection programs is limited to those of Microcystis virus Ma-LMM01, which was a narrow host range in which it can escape from the highly abundant host defense systems. Our metagenomic approaches unveiled the cooccurrence of narrow- and broad-host-range Microcystis viruses, which included fifteen viral genomic fragments from Microcystis blooms that were classified into three groups. Interestingly, Microcystis antiviral defense genes were expressed against viral infection in the environment, unlike what was seen in a culture experiment with Ma-LMM01. Given that viruses with a broad host range often induce antiviral responses within alternative hosts, our findings suggest that antiviral responses inhibit viral reproduction, especially that of broad-range viruses like those in group II. This paper augments our understanding of the interactions between M. aeruginosa and its viruses and fills an important knowledge gap.

SUBMITTER: Morimoto D

PROVIDER: S-EPMC6715842 | biostudies-literature |

REPOSITORIES: biostudies-literature

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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.

Project description:Microcystis aeruginosa forms massive blooms in eutrophic freshwaters, where it is constantly exposed to lytic cyanophages. Unlike other marine cyanobacteria, M. aeruginosa possess remarkably abundant and diverse potential antiviral defense genes. Interestingly, T4-like cyanophage Ma-LMM01, which is the sole cultured lytic cyanophage infecting M. aeruginosa, lacks the host-derived genes involved in maintaining host photosynthesis and directing host metabolism that are abundant in other marine cyanophages. Based on genomic comparisons with closely related cyanobacteria and their phages, Ma-LMM01 is predicted to employ a novel infection program that differs from that of other marine cyanophages. Here, we used RNA-seq technology and in silico analysis to examine transcriptional dynamics during Ma-LMM01 infection to reveal host transcriptional responses to phage infection, and to elucidate the infection program used by Ma-LMM01 to avoid the highly abundant host defense systems. Phage-derived reads increased only slightly at 1 h post-infection, but significantly increased from 16% of total cellular reads at 3 h post-infection to 33% of all reads by 6 h post-infection. Strikingly, almost none of the host genes (0.17%) showed a significant change in expression during infection. However, like other lytic dsDNA phages, including marine cyanophages, phage gene dynamics revealed three expression classes: early (host-takeover), middle (replication), and late (virion morphogenesis). The early genes were concentrated in a single ?5.8-kb window spanning 10 open reading frames (gp054-gp063) on the phage genome. None of the early genes showed homology to the early genes of other T4-like phages, including known marine cyanophages. Bacterial RNA polymerase (?70) recognition sequences were also found in the upstream region of middle and late genes, whereas phage-specific motifs were not found. Our findings suggest that unlike other known T4-like phages, Ma-LMM01 achieves three sequential gene expression patterns with no change in host promoter activity. This type of infection that does not cause significant change in host transcriptional levels may be advantageous in allowing Ma-LMM01 to escape host defense systems while maintaining host photosynthesis.

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Cooccurrence of Broad- and Narrow-Host-Range Viruses Infecting the Bloom-Forming Toxic Cyanobacterium Microcystis aeruginosa.

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