Pyrite stimulates the growth and sulfur oxidation capacity of anoxygenic phototrophic sulfur bacteria in euxinic environments

Abstract

Anoxygenic phototrophic sulfur bacteria flourish in contemporary and ancient euxinic environments, driving the biogeochemical cycles of carbon and sulfur. However, it is unclear how these strict anaerobes meet their high demand for iron in iron-depleted environments. Here, we report that pyrite, a widespread and highly stable iron sulfide mineral in anoxic, low-temperature environments, can support the growth and metabolic activity of anoxygenic phototrophic sulfur bacteria by serving as the sole iron source under iron-depleted conditions. Transcriptomic and proteomic analyses revealed that pyrite addition substantially up-regulated genes and protein expression involved in photosynthesis, sulfur metabolism, and biosynthesis of organics. Anoxic microbial oxidation of pyritic sulfur and consequent destabilization of the pyrite structure were postulated to facilitate microbial iron acquisition. These findings advance our understanding of the survival strategies of anaerobes in iron-depleted environments and are important for revealing the previously underappreciated bioavailability of pyritic iron in anoxic environments and anoxic weathering of pyrite.