Distribution of Arsenic Resistance Genes in Prokaryotes

Abstract

Arsenic is a metalloid that occurs naturally in aquatic and terrestrial environments. The high toxicity of arsenic derivatives converts this element in a serious problem of public health worldwide. There is a global arsenic geocycle in which microbes play a relevant role. Ancient exposure to arsenic derivatives, both inorganic and organic, has represented a selective pressure for microbes to evolve or acquire diverse arsenic resistance genetic systems. In addition, arsenic compounds appear to have been used as a toxin in chemical warfare for a long time selecting for an extended range of arsenic resistance determinants. Arsenic resistance strategies rely mainly on membrane transport pathways that extrude the toxic compounds from the cell cytoplasm. The ars operons, first discovered in bacterial R-factors almost 50 years ago, are the most common microbial arsenic resistance systems. Numerous ars operons, with a variety of genes and different combinations of them, populate the prokaryotic genomes, including their accessory plasmids, transposons, and genomic islands. Besides these canonical, widespread ars gene clusters, which confer resistance to the inorganic forms of arsenic, additional genes have been discovered recently, which broadens the spectrum of arsenic tolerance by detoxifying organic arsenic derivatives often used as toxins. This review summarizes the presence, distribution, organization, and redundance of arsenic resistance genes in prokaryotes.

Keywords: ars operon; arsenic; efflux; mine railings; remediation; resistance.

FIGURE 1

Distribution of ars genes in arsenic-resistant prokaryotes. Genetic organization of ars operons from various arsenic resistant bacterial strains. Arrows represent open reading frames and orientation of transcription. Chr, chromosomal genes. Gene descriptions and references associated are given in the text.

FIGURE 2

MAs(III): a primordial antibiotic. In communities of soil microbes some bacteria such as Rhodopseudomonas palustris carry the arsM gene for the As(III) SAM methyltransferase, producing highly toxic MAs(III). This trivalent organoarsenical has antibiotic-like properties. Other soil bacteria carry genes for MAs(III) resistance. Some, such as Bacillus MD1, have the arsI gene for the ArsI C-As lyase enzyme that confers resistance to MAs(III) by degrading it into As(III) and formaldehyde. Yet other soil bacteria such as Pseudomonas putida have a gene encoding ArsH, a flavoprotein that uses NADP+ to oxidize MAs(III) to MAs(V), thus conferring resistance. Finally, other bacteria such as Campylobacter jejuni, which inhabits the intestinal track of poultry and other farm animals, carry the arsP gene. ArsP is a MAs(III) efflux permease that extrudes trivalent organoarsenicals from cells, conferring resistance. The crystal structures of the relevant enzymes are shown next to their reactions (Li et al., 2016b).

FIGURE 3

Common pathways in arsenic resistance on prokaryotes. Under aerobic conditions, As(V) enters the cell via phosphate uptake systems (here PstA, PstB, PstC, and PhoS). As(V) is then reduced by the arsenate reductase ArsC to As(III). Although As(III) is more toxic than As(V), As(III) can easily be distinguished from phosphate, which is very similar to As(V). As(III) can also directly be taken up by various aquaglyceroporins such as GlpF from E. coli. As(III) can then be translocated across the cytoplasmic membrane via Acr3 or ArsB using the proton motive force (PMF). Alternatively, As(III) can be bound by the As(III)-binding chaperone ArsD and delivered to the ATP-dependent ArsAB efflux pump. Organic arsenic compounds such as MMA(III) and Roxarsone can also be pumped out by the ArsP transporter.