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Comparative protein expression in different strains of the bloom-forming cyanobacterium Microcystis aeruginosa.

ABSTRACT: Toxin production in algal blooms presents a significant problem for the water industry. Of particular concern is microcystin, a potent hepatotoxin produced by the unicellular freshwater species Microcystis aeruginosa. In this study, the proteomes of six toxic and nontoxic strains of M. aeruginosa were analyzed to gain further knowledge in elucidating the role of microcystin production in this microorganism. This represents the first comparative proteomic study in a cyanobacterial species. A large diversity in the protein expression profiles of each strain was observed, with a significant proportion of the identified proteins appearing to be strain-specific. In total, 475 proteins were identified reproducibly and of these, 82 comprised the core proteome of M. aeruginosa. The expression of several hypothetical and unknown proteins, including four possible operons was confirmed. Surprisingly, no proteins were found to be produced only by toxic or nontoxic strains. Quantitative proteome analysis using the label-free normalized spectrum abundance factor approach revealed nine proteins that were differentially expressed between toxic and nontoxic strains. These proteins participate in carbon-nitrogen metabolism and redox balance maintenance and point to an involvement of the global nitrogen regulator NtcA in toxicity. In addition, the switching of a previously inactive toxin-producing strain to microcystin synthesis is reported.

SUBMITTER: Alexova R

PROVIDER: S-EPMC3186190 | biostudies-literature | 2011 Sep

REPOSITORIES: biostudies-literature

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Comparative protein expression in different strains of the bloom-forming cyanobacterium Microcystis aeruginosa.

Alexova Ralitza R Haynes Paul A PA Ferrari Belinda C BC Neilan Brett A BA

Molecular & cellular proteomics : MCP 20110524 9

Toxin production in algal blooms presents a significant problem for the water industry. Of particular concern is microcystin, a potent hepatotoxin produced by the unicellular freshwater species Microcystis aeruginosa. In this study, the proteomes of six toxic and nontoxic strains of M. aeruginosa were analyzed to gain further knowledge in elucidating the role of microcystin production in this microorganism. This represents the first comparative proteomic study in a cyanobacterial species. A larg ...[more]

PMID: 21610102

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Project description:The frequency and intensity of cyanobacterial blooms are increasing worldwide. Interactions between toxic cyanobacteria and aquatic microorganisms need to be critically evaluated to understand microbial drivers and modulators of the blooms. In this study, we applied 16S/18S rRNA gene sequencing and metabolomics analyses to measure the microbial community composition and metabolic responses of the cyanobacterium Microcystis aeruginosa in a coculture system receiving dissolved inorganic nitrogen and phosphorus (DIP) close to representative concentrations in Lake Taihu, China. M. aeruginosa secreted alkaline phosphatase using a DIP source produced by moribund and decaying microorganisms when the P source was insufficient. During this process, M. aeruginosa accumulated several intermediates in energy metabolism pathways to provide energy for sustained high growth rates and increased intracellular sugars to enhance its competitive capacity and ability to defend itself against microbial attack. It also produced a variety of toxic substances, including microcystins, to inhibit metabolite formation via energy metabolism pathways of aquatic microorganisms, leading to a negative effect on bacterial and eukaryotic microbial richness and diversity. Overall, compared with the monoculture system, the growth of M. aeruginosa was accelerated in coculture, while the growth of some cooccurring microorganisms was inhibited, with the diversity and richness of eukaryotic microorganisms being more negatively impacted than those of prokaryotic microorganisms. These findings provide valuable information for clarifying how M. aeruginosa can potentially modulate its associations with other microorganisms, with ramifications for its dominance in aquatic ecosystems.IMPORTANCE We measured the microbial community composition and metabolic responses of Microcystis aeruginosa in a microcosm coculture system receiving dissolved inorganic nitrogen and phosphorus (DIP) close to the average concentrations in Lake Taihu. In the coculture system, DIP is depleted and the growth and production of aquatic microorganisms can be stressed by a lack of DIP availability. M. aeruginosa could accelerate its growth via interactions with specific cooccurring microorganisms and the accumulation of several intermediates in energy metabolism-related pathways. Furthermore, M. aeruginosa can decrease the carbohydrate metabolism of cooccurring aquatic microorganisms and thus disrupt microbial activities in the coculture. This also had a negative effect on bacterial and eukaryotic microbial richness and diversity. Microcystin was capable of decreasing the biomass of total phytoplankton in aquatic microcosms. Overall, compared to the monoculture, the growth of total aquatic microorganisms is inhibited, with the diversity and richness of eukaryotic microorganisms being more negatively impacted than those of prokaryotic microorganisms. The only exception is M. aeruginosa in the coculture system, whose growth was accelerated.

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 (σ70) 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.

Dataset Information

Comparative protein expression in different strains of the bloom-forming cyanobacterium Microcystis aeruginosa.

Publications

Comparative protein expression in different strains of the bloom-forming cyanobacterium Microcystis aeruginosa.

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