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

Abstract

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, U.S. 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 ([H2As(III)S(-II)O2](-)), formed as an intermediate by abiotic reaction of arsenite with sulfide. We now report that this species is monothioarsenate ([HAs(V)S(-II)O3](2-)) as revealed by X-ray absorption spectroscopy. Monothioarsenate forms by abiotic reaction of arsenite with zerovalent 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 zerovalent sulfur or sulfate while concurrently reducing the central arsenic atom (As(V)) 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.

Linking Genes to Microbial Biogeochemical Cycling: Lessons from Arsenic

“…These play a significant role in the arsenic biochemical cycle in sulfidic geothermal environments. 74–76 Thioarsenates are transformed to As(V) and/or As(III) via exposing to oxidizing agents or increased pH, 77 by biological conversion by sulfur-oxidizing bacteria, 75,78 or by abiotic decomposition (desulfidation) with subsequent biological oxidation. 77,79 Thioarsenates contain reduced S 2− and oxidized As(V).…”

“…81 Recently, the haloalkaliphilic bacterium MLMS-1 can grow chemolithotrophically by oxidizing the S 2− of monothioarsenate to S 0 or SO 4 2− , while concurrently reducing As(V) to As(III). 78 In summary, various microbes have evolved to utilize thioarsenates that are widespread in sulfidic environments.…”

Thioarsenate Formation Coupled with Anaerobic Arsenite Oxidation by a Sulfate-Reducing Bacterium Isolated from a Hot Spring

“…in which arsenate reacted with sulfide, leading to the formation of thioarsenate (Planer-Friedrich et al, 2015). The reactant arsenate could be extant or derived from arsenite oxidation.…”

“…All experimental treatments were performed in triplicate. Liquid sampling for arsenic measurement was performed with aseptic syringes in an anaerobic chamber according to a previous method (Planer-Friedrich et al, 2015). …”

“…and Sulfurihydrogenibium spp. (Planer-Friedrich et al, 2015). However, little is known about which microbial group was involved in the observed thioarsenate species transformation.…”