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

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.