Looking for the mechanism of arsenate respiration in an arsenate-dependent growing culture ofFusibactersp. strain 3D3, independent of ArrAB

Abstract

Abstract The literature has reported the isolation of arsenate-dependent growing (ADG) microorganisms which lack a canonical homolog for respiratory arsenate reductase, ArrAB. We recently isolated an ADG bacterium from arsenic-bearing environments in Northern Chile, Fusibacter sp. strain 3D3 ( Fas ) and studied the arsenic metabolism in this Gram-positive isolate. Features of Fas deduced from genome analysis and comparative analysis with other arsenic-reducing microorganisms revealed the lack of ArrAB coding genes and the occurrence of two arsC genes encoding for putative cytoplasmic arsenate reductases named ArsC-1 and ArsC-2. Interestingly, ArsC-1 and ArsC-2 belong to the thioredoxin-coupled family (because of the redox-active disulfide protein used as reductant), but they conferred differential AsV resistance to the E. coli WC3110 Δ arsC strain. PCR experiments confirmed the absence of arrAB genes and results obtained using uncouplers revealed that Fas growth is linked to the proton gradient. In addition, Fas harbors ferredoxin-NAD + oxidoreductase (Rnf) coding genes. These are key molecular markers of a recently discovered flavin-based electron bifurcation mechanism involved in energy conservation, mainly in anaerobic metabolisms regulated by the cellular redox state and mostly associated with cytoplasmic enzyme complexes. At least three electron-bifurcating flavoenzyme complexes were evidenced in Fas , some of them shared in conserved genomic regions by other members of the Fusibacter genus. These physiological and genomic findings permit us to hypothesize the existence of an uncharacterized arsenate-dependent growth metabolism regulated by the cellular redox state in Fusibacter genus.