Diel regulation of hydrogen peroxide defenses by open ocean microbial communities

Abstract

Hydrogen peroxide (HOOH) is omnipresent in natural waters. Given that sunlight is the primary source of HOOH, we investigated the relationship between time of day and microbial HOOH degradation. Genes encoding HOOHdegrading enzymes were significantly more abundant during the day in ocean metatranscriptomes. While bacterial catalase-peroxidases were the most abundant transcripts, the abundance of algal peroxidases, along with the insensitivity of HOOH degradation rates to antibiotic treatment in our incubations, suggested that eukaryotic microorganisms were also important scavengers of HOOH. Phylogenetic placement of transcripts for HOOH degrading enzymes suggested that different taxa expressed these enzymes during the day than during the night. We also measured HOOH concentrations over a 24 h period in the South Pacific, and simultaneously conducted bottle incubations to measure HOOH dark degradation rates. Fitting these data to a dynamic model confirmed that the ability of the microbial community to degrade HOOH during the day increased, with peak HOOH removal rates occurring in late afternoon coincident with the highest HOOH concentrations. Collectively, these data suggest that even in dilute HOOH environments, there is a dynamic diel response to HOOH, and that the open ocean microbial community is complicit in its cross-protection of Prochlorococcus and other HOOH-sensitive taxa.