Manganese oxide biomineralization is a social trait protecting against nitrite toxicity

Abstract

Manganese bio-mineralization by oxidation is a costly but, still, widespread process among bacteria and fungi. While certain potential advantages of manganese oxidation have been suggested, to date there is no conclusive experimental evidence for, how and if this process impacts microbial fitness in the environment. Here we show how a model organism for manganese oxidation, Roseobacter sp. AzwK-3b, is growth-inhibited by nitrite, and that this inhibition is mitigated when manganese is added to the culture medium. We show that manganese-mediated mitigation of nitrite-inhibition is dependent on the culture inoculum size, with larger inocula being able to withstand higher concentrations of nitrite stress. Furthermore, the bio-mineralized manganese oxide (MnOX) forms granular precipitates in the culture, rather than sheaths around individual cells. These findings support the notion that MnOX is a shared community product that improves the cultures survival against nitrite-stress. We show that the mechanistic basis of the MnOX effect involves both its ability to catalyze nitrite oxidation into (non-toxic) nitrate under physiological conditions, and its potential role in influencing redox chemistry around reactive oxygen species (ROS). Taken together, these results provide for the first direct evidence of improved microbial fitness by MnOX deposition in an ecological setting, i.e. mitigation of nitrite toxicity, and point to a key role of MnOX in handling stresses arising from ROS. These findings could be of general relevance for all organisms oxidizing manganese, allowing them to offset costs associated with extracellular bio-mineralization.