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. 2022 Jul 26;88(14):e0254421.
doi: 10.1128/aem.02544-21. Epub 2022 Jul 5.

Heterotrophic Bacteria Dominate Catalase Expression during Microcystis Blooms

Derek J Smith  1 , Michelle A Berry  2 , Rose M Cory  1 , Thomas H Johengen  3 , George W Kling  2 , Timothy W Davis  4 , Gregory J Dick  1   3
Affiliations

Heterotrophic Bacteria Dominate Catalase Expression during Microcystis Blooms

Derek J Smith et al. Appl Environ Microbiol. .

Abstract

In the oligotrophic oceans, key autotrophs depend on "helper" bacteria to reduce oxidative stress from hydrogen peroxide (H2O2) in the extracellular environment. H2O2 is also a ubiquitous stressor in freshwaters, but the effects of H2O2 on autotrophs and their interactions with bacteria are less well understood in freshwaters. Naturally occurring H2O2 in freshwater systems is proposed to impact the proportion of microcystin-producing (toxic) and non-microcystin-producing (nontoxic) Microcystis in blooms, which influences toxin concentrations and human health impacts. However, how different strains of Microcystis respond to naturally occurring H2O2 concentrations and the microbes responsible for H2O2 decomposition in freshwater cyanobacterial blooms are unknown. To address these knowledge gaps, we used metagenomics and metatranscriptomics to track the presence and expression of genes for H2O2 decomposition by microbes during a cyanobacterial bloom in western Lake Erie in the summer of 2014. katG encodes the key enzyme for decomposing extracellular H2O2 but was absent in most Microcystis cells. katG transcript relative abundance was dominated by heterotrophic bacteria. In axenic Microcystis cultures, an H2O2 scavenger (pyruvate) significantly improved growth rates of one toxic strain while other toxic and nontoxic strains were unaffected. These results indicate that heterotrophic bacteria play a key role in H2O2 decomposition in Microcystis blooms and suggest that their activity may affect the fitness of some Microcystis strains and thus the strain composition of Microcystis blooms but not along a toxic versus nontoxic dichotomy. IMPORTANCE Cyanobacterial harmful algal blooms (CHABs) threaten freshwater ecosystems globally through the production of toxins. Toxin production by cyanobacterial species and strains during CHABs varies widely over time and space, but the ecological drivers of the succession of toxin-producing species remain unclear. Hydrogen peroxide (H2O2) is ubiquitous in natural waters, inhibits microbial growth, and may determine the relative proportions of Microcystis strains during blooms. However, the mechanisms and organismal interactions involved in H2O2 decomposition are unexplored in CHABs. This study shows that some strains of bloom-forming freshwater cyanobacteria benefit from detoxification of H2O2 by associated heterotrophic bacteria, which may impact bloom development.

Keywords: CHABs; Microcystis; catalase; hydrogen peroxide; metagenomics; metatranscriptomics; peroxidase.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

FIG 1
FIG 1
Temporal and spatial trends in the relative abundance of catalase and peroxidase genes in the 2014 western Lake Erie cyanobacterial bloom metagenomes are not correlated with concentrations of phycocyanin, particular microcystins, or H2O2. Genes with KEGG orthology (KO) annotations for catalase-peroxidase (katG) and alkyl hydroperoxide reductase subunit C (ahpC) had the highest relative abundances. The relative abundance of catalase and peroxidase genes shown is the total of all genes with the specified KEGG orthology ID in metagenomes from the >100-μm particle size fraction at each station. Read counts are normalized to the length of the matching gene in the database and to the number of reads that mapped to bacterial rpoB, encoding the beta subunit of RNA polymerases. Error bars on H2O2 concentrations show the standard error of technical replicate measurements (n = 3).
FIG 2
FIG 2
Temporal and spatial trends in the relative abundance of total katG and ahpC transcripts in particle- and phytoplankton-attached microbial communities show qualitative patterns with H2O2 concentration. The relative abundance of catalase and peroxidase genes shown is the total of all genes with the specified KEGG orthology (KO) ID in metatranscriptomes from the >100-μm particle size fraction at each station. Read counts are normalized to the length of the matching gene in the database and to the number of reads that mapped to bacterial rpoB, encoding the beta subunit of RNA polymerases. Relative abundance of ahpC is shown separately in the middle panel because it was 2 orders of magnitude higher than the combined total of the other genes. Error bars on H2O2 concentrations show the standard error of technical replicate measurements (n = 3).
FIG 3
FIG 3
Genes and transcripts encoding KatG in the 2014 western Lake Erie cyanobacterial bloom were from a diverse community of microbes, and katG from Microcystis did not dominate total katG reads. katG reads were summed by taxonomic assignment. For each sample, only taxa that had percent abundances higher than 5% of the total katG reads in the given sample are shown; the remaining white space is made up of taxa with katG that had a percent abundance below 5%. Dates without bars indicate that no data are present for the given combination of date and station. metaG, metagenome samples; metaT, metatranscriptome samples.
FIG 4
FIG 4
Spatial and temporal variation in Microcystis katG abundance relative to Microcystis rpoB in metagenomes and metatranscriptomes from the 2014 western Lake Erie cyanobacterial bloom. (A) Low and decreasing katG/rpoB ratios with time suggest that a minority of Microcystis genomes in the 2014 bloom have katG and fewer Microcystis genomes have katG in the late summer and fall. (B) There are no quantitative or qualitative relationships between the relative abundance of Microcystis katG transcripts and H2O2 concentrations.
FIG 5
FIG 5
Microcystis ahpC was abundant in most particle- and phytoplankton-associated metagenomic samples and dominated particle- and phytoplankton-associated ahpC transcripts in the 2014 western Lake Erie cyanobacterial bloom, but Microcystis ahpC was less abundant in whole water metagenome samples. ahpC reads were summed by taxonomic assignment. For each sample, only taxa that had percent abundances higher than 2% of the total ahpC reads in the given sample are shown; the remaining white space is made up of taxa with ahpC that had a percent abundance below 2%. Dates without bars indicate that no data are present for the given combination of date and station. metaG, metagenome samples; metaT, metatranscriptome samples.
FIG 6
FIG 6
(A) Small differences in cell density between pyruvate and control treatments and the decomposition of initially high, but environmentally relevant, H2O2 concentrations suggest that Microcystis does not require help degrading H2O2 under the experimental conditions despite lacking katG. Error bars depict 95% confidence intervals of biological triplicates. (B) Some Microcystis strains had significant (P < 0.05) improvements in maximum growth rates when cultured with pyruvate, suggesting a benefit from receiving help with H2O2 decomposition. Strain toxigenicity is not an indicator of whether a strain benefits from help decomposing H2O2. Significance was determined with Welch’s two-sided t test. (C) In sterile growth medium, H2O2 concentrations increase over time rather than decrease. Error bars depict 95% confidence intervals of three technical replicates.
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