Anaerobic Chemolithotrophic Growth of the Haloalkaliphilic Bacterium Strain MLMS‑1 by Disproportionation of Monothioarsenate

B. Planer-Friedrich, C. Härtig, R. Lohmayer, E. Suess, S. H. McCann, R. Oremland

A novel chemolithotrophic metabolism based on a mixed arsenic-sulfur species has been discovered for the anaerobic deltaproteobacterium, strain MLMS-1, a haloalkaliphile isolated from Mono Lake, California, USA. Strain MLMS-1 is the first reported obligate arsenate-respiring chemoautotroph which grows by coupling arsenate reduction to arsenite with the oxidation of sulfide to sulfate. In that pathway the formation of a mixed arsenic-sulfur species was reported. That species was assumed to be monothioarsenite ([H2AsIIIS-IIO2]-), formed as an intermediate by abiotic reaction of arsenite with sulfide. We now report that this species is monothioarsenate ([HAsVS-IIO3]2-) as revealed by X-ray absorption spectroscopy. Monothioarsenate forms by abiotic reaction of arsenite with zero-valent sulfur. Monothioarsenate is kinetically stable under a wide range of pH and redox conditions. However, it was metabolized rapidly by strain MLMS-1 when incubated with arsenate. Incubations using monothioarsenate confirmed that strain MLMS-1 was able to grow (µ = 0.017 h-1) on this substrate via a disproportionation reaction by oxidizing the thio-group-sulfur (S-II) to zero-valent sulfur or sulfate while concurrently reducing the central arsenic atom (AsV) to arsenite. Monothioarsenate disproportionation could be widespread in nature beyond the already studied arsenic and sulfide rich hot springs and soda lakes where it was discovered.