Linkage between bacterial community-mediated hydrogen peroxide detoxification and the growth of Microcystis aeruginosa

Abstract

Microcystis aeruginosa, an important cyanobloom-forming cyanobacterium, is sensitive to the high light intensity and consequent oxidative stress. Based on our genomic and transcriptomic analyses of H2O2-treated cells, many genes involved in photosynthesis, Calvin cycle, and microcystin synthesis were downregulated, whereas several toxin-antitoxin genes, DNA repair genes, and H2O2-defense systems such as peroxiredoxins and glutathione synthesis were upregulated. Axenic M. aeruginosa was then co-cultured with synthetic bacterial communities collected from 15 different freshwater samples with exhibiting different degrees of H2O2-production and catalase activities. Our analyses indicated that H2O2-resistant bacterial communities favored the growth and photosynthetic activity of M. aeruginosa cells under either H2O2 treatment or high light conditions. Nanopore-based bacterial community analyses indicated that these growth-promoting effects were likely attributable to a high proportion of Alphaproteobacteria (e.g., Brevundimonas and Ochrobactrum species), which protected M. aeruginosa cells from H2O2 toxicity. Further, these bacterial communities exhibited higher catalase activity levels and faster O2 production rates upon H2O2 detoxification. Taken together, our findings newly suggest that the occurrence of catalase-less M. aeruginosa blooms is largely influenced by the surrounding microbiota during high light and organic-rich conditions.