Heterotrophic Bacteria Dominate Catalase Expression during Microcystis Blooms

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. 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.

Automated summary

Cyanobacterial harmful algal blooms (CHABs) pose a global threat to freshwater ecosystems due to toxin production. This study reveals the key role of heterotrophic bacteria in decomposing hydrogen peroxide (H2O2) and suggests their activity may impact the fitness and strain composition of CHABs. The dichotomy of toxin-producing and non-toxin-producing strains may not drive the succession of toxin-producing species.