Natural concentrations of hydrogen peroxide (H2O2) as low as 200 nM have been shown to impact the fitness of microbes implicated in critical biogeochemical functions and have been hypothesized to impact microcystin concentrations during cyanobacterial harmful algae blooms (CHABs). H2O2 is a reactive oxygen species that is formed naturally in aquatic ecosystems by photochemical reactions with chromophoric dissolved organic matter (CDOM) and biologically as a by-product of oxygenic photosynthesis and aerobic respiration. H2O2 causes oxidative damage to biomolecules and inhibits protein synthesis. Therefore, it is a critical adaptation of aerobically growing organisms to scavenge both endo- and exogenous H2O2. H2O2 concentrations ranging from 690 (± 40 nM) to 20 nM (± 10 nM) have been observed in western Lake Erie CHABs, which is within the range at which negative impacts on microbial fitness have been observed. The patterns in H2O2 concentrations observed in western Lake Erie cannot be explained by photochemical sources alone, suggesting that shifts in the balance between microbial sources and sinks are driving the observed patterns in H2O2 concentration during the CHAB. To investigate this hypothesis, the abundance and expression of genes encoding catalases and peroxidases, the dominant sinks of H2O2in aquatic ecosystems, in a western Lake Erie CHAB were measured using metagenomics and metatranscriptomics.
The most abundant catalase and peroxidase genes in the metagenome and metatranscriptome were katG, encoding the bifunctional catalase-peroxidase enzymes, and ahpC, encoding alkyl hydroperoxidase; these are the dominant enzymes for scavenging exogenous and endogenous H2O2, respectively. Relative katG expression was highest directly after peak H2O2 concentrations, suggesting that microbial communities are responding to elevated concentrations of H2O2 and, in turn, leading to an increased sink and declining concentrations of H2O2. Relative expression of ahpC was highest in the late phase of the bloom as algal pigments were declining, suggesting a reduced source of H2O2 into the environment. Together, these lines of evidence support the hypothesis that microbial functions are shaping H2O2 dynamics in the CHAB. In addition, metagenomic assembled genomes from the 2014 western Lake Erie CHAB indicate that Microcystis lacks katG, suggesting that Microcystis depends on katG expression by other colony-associated bacteria to mitigate oxidative stress caused by exogenous H2O2. This research provides new insights at the genetic level on how microbial interactions are driving H2O2 dynamics during CHABs, which may impact CHAB community structure and function.