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

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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,Fusibactersp. strain 3D3 (Fas) and studied the arsenic metabolism in this Gram-positive isolate. Features ofFasdeduced from genome analysis and comparative analysis with other arsenic-reducing microorganisms revealed the lack of ArrAB coding genes and the occurrence of twoarsCgenes 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 theE. coliWC3110 ΔarsCstrain. PCR experiments confirmed the absence ofarrABgenes and results obtained using uncouplers revealed thatFasgrowth is linked to the proton gradient. In addition,Fasharbors 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 inFas, some of them shared in conserved genomic regions by other members of theFusibactergenus. These physiological and genomic findings permit us to hypothesize the existence of an uncharacterized arsenate-dependent growth metabolism regulated by the cellular redox state inFusibactergenus.

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