Sulfuriferula spp. from sulfide mineral weathering environments have diverse sulfur- and iron-cycling capabilities

Abstract

Microorganisms are important catalysts for the oxidation of reduced inorganic sulfur compounds. One environmentally important source of reduced sulfur is metal sulfide minerals that occur in economic mineral deposits and mine waste. Previous research found that Sulfuriferula spp. were abundant and active in long-term weathering experiments with simulated waste rock and tailings from the Duluth Complex, Northern Minnesota. We therefore isolated several strains of Sulfuriferula spp. from these long-term experiments and characterized their metabolic and genomic properties to provide insight into microbe-mineral interactions and the microbial biogeochemistry in these and other moderately acidic to circumneutral environments. The Sulfuriferula strains are all obligate chemolithoautotrophs capable of oxidizing inorganic sulfur compounds and ferrous iron. The strains grew over different pH ranges, but all grew between pH 4.5-7, matching the weathering conditions of the Duluth Complex rocks. All strains grew on the iron-sulfide mineral pyrrhotite (Fe1-xS, 0 < x < 0.125) as the sole energy source, as well as hydrogen sulfide and thiosulfate, which are products of sulfide mineral breakdown. Despite their metabolic similarities, each strain encodes a distinct pathway for the oxidation of reduced inorganic sulfur compounds as well as differences in nitrogen metabolism that reveal diverse genomic capabilities among the group. Our results show that Sulfuriferula spp. are primary producers that likely play a role in sulfide mineral breakdown in moderately acidic to circumneutral mine waste, and the metabolic diversity within the genus likely explains their success in sulfide mineral-rich and other sulfidic environments. ImportanceMetal sulfide minerals such as pyrite and pyrrhotite are one of the main sources of reduced sulfur in the global sulfur cycle. The chemolithotrophic microorganisms that break down these minerals in natural and engineered settings are catalysts for biogeochemical sulfur cycling and have important applications in biotechnological processes such as biomining or bioremediation. Sulfuriferula is a recently described genus of sulfur oxidizing bacteria that are abundant primary producers in diverse terrestrial environments, including waste rock and tailings from metal mining operations. In this study, we explored the genomic and metabolic properties of new isolates from this genus, and the implications for their ecophysiology and biotechnological potential in ore and waste from economic mineral deposits.