ArxA From Azoarcus sp. CIB, an Anaerobic Arsenite Oxidase From an Obligate Heterotrophic and Mesophilic Bacterium.

Gonzalo Durante-Rodríguez,Elena Alonso-Fernandes,Manuel Carmona,Eduardo Díaz,María Nieves Fernández-Muñiz,Helga Fernández-Llamosas,Riansares Muñoz-Olivas

doi:10.3389/fmicb.2019.01699

Gonzalo Durante-Rodríguez, Elena Alonso-Fernandes + Show 5 more

Open Access

https://doi.org/10.3389/fmicb.2019.01699

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Abstract

Arsenic is a toxic element widely distributed in nature, but numerous bacteria are able to resist its toxicity mainly through the ars genes encoding an arsenate reductase and an arsenite efflux pump. Some “arsenotrophic” bacteria are also able to use arsenite as energy supplier during autotrophic growth by coupling anaerobic arsenite oxidation via the arx gene products to nitrate respiration or photosynthesis. Here, we have demonstrated that Azoarcus sp. CIB, a facultative anaerobic β-proteobacterium, is able to resist arsenic oxyanions both under aerobic and anaerobic conditions. Genome mining, gene expression, and mutagenesis studies revealed the presence of a genomic island that harbors the ars and arx clusters involved in arsenic resistance in strain CIB. Orthologous ars clusters are widely distributed in the genomes of sequenced Azoarcus strains. Interestingly, genetic and metabolic approaches showed that the arx cluster of the CIB strain encodes an anaerobic arsenite oxidase also involved in the use of arsenite as energy source. Hence, Azoarcus sp. CIB represents the prototype of an obligate heterotrophic bacterium able to use arsenite as an extra-energy source for anaerobic cell growth. The arsenic island of strain CIB supports the notion that metabolic and energetic skills can be gained by genetic mobile elements.

Highlights

Arsenic (As) is an element that is widely distributed in nature, either present naturally as an element of the soil composition or due to its release from anthropogenic sources
We have identified the genetic determinants involved in arsenic resistance in a member of the Azoarcus genus
Whereas arsenic resistance is widely extended in bacteria, the ability to use arsenite as energy source has been mainly related to extremophile autotrophic bacteria that reside in environments highly contaminated with arsenic oxyanions

Summary

Introduction

Arsenic (As) is an element that is widely distributed in nature, either present naturally as an element of the soil composition or due to its release from anthropogenic sources. Resistance to arsenic is widely spread among bacteria, and different resistance strategies, e.g., As uptake selectivity, As(III) oxidation, As(V) reduction, efflux of all As compounds, As methylation and volatilization, Arsenite Oxidase of Azoarcus CIB have been reported (Zhu et al, 2014). The molecular basis of some of the mechanisms of arsenic resistance has been well-studied (Mukhopadhyay et al, 2002; Rosen, 2002). The most common and widely distributed As resistance mechanism, i.e., arsenate reduction coupled to arsenite extrusion, is encoded by the ars genes present in many bacteria and archaea, where they show remarkable diversity in their sequence and genomic organization (Mukhopadhyay and Rosen, 2002), and they can be plasmid borne or chromosomally encoded (Oden et al, 1994; Cai et al, 1998)

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