Unsuspected Diversity of Arsenite-Oxidizing Bacteria as Revealed by Widespread Distribution of theaoxBGene in Prokaryotes

Abstract

In this study, new strains were isolated from an environment with elevated arsenic levels, Sainte-Marieaux-Mines (France), and the diversity of aoxB genes encoding the arsenite oxidase large subunit was investigated. The distribution of bacterial aoxB genes is wider than what was previously thought. AoxB subfamilies characterized by specific signatures were identified. An exhaustive analysis of AoxB sequences from this study and from public databases shows that horizontal gene transfer has likely played a role in the spreading of aoxB in prokaryotic communities.Arsenic, which is one of the most toxic metalloids, is distributed ubiquitously but not uniformly around the world. Levels of arsenic differ considerably from one geographical region to another, depending on the geochemical characteristics of the soil (natural contamination) and the industrial activities carried out in the vicinity (anthropogenic contamination) (22). In aquatic environments, arsenic occurs mainly in the form of the inorganic species arsenate [As(V)] and arsenite [As(III)]; the latter species, which is more bioavailable, is usually thought to have more-toxic effects on prokaryotes than As(V) (34). As(III) oxidation leads to the formation of the less available form As(V), which can either precipitate with iron [Fe(III)] or be adsorbed by ferrihydrite. The oxidation process may be mediated by microbial activities, which contribute to the natural remediation processes observed in contaminated environments (21,26,27,34). Consequently, bioprocesses for the treatment of arsenic-contaminated waters have been developed based on the precipitation or adsorption of the As(V) produced by bacteria (4, 9, 21). Some well-known prokaryotes oxidize As(III) into As(V) under aerobic (e.g., Herminiimonas arsenicoxydans, Thiomonas spp., or Rhizobium sp. strain NT26) or anaerobic (e.g., Alkalilimnicola ehrlichii) conditions as part of a detoxification process (12,17,31,32,39). Some chemolithotrophs also use arsenite as an electron donor (e.g., Rhizobium sp. strain NT26 or Thiomonas arsenivorans) (5, 32). The aerobic arsenite oxidases involved in such processes are heterodimers consisting of a large subunit with a molybdenum center and a [3Fe-4S] cluster (AroA, AsoA, and AoxB) and a small subunit containing a Rieske-type [2Fe-2S] cluster (AroB, AsoB, and AoxA) (1, 13). The large subunit in these enzymes is similar to that found in other members of the dimethyl sulfoxide (DMSO) reductase family of molybdenum enzymes but is clearly phylogenetically divergent from the respiratory arsenate reductases (ArrA) or other proteins of the DMSO reductase family of molybdenum oxidoreductases, such as the new arsenite reductase described recently for Alkalilimnicola ehrlichii (25,31,40).aox genes have been identified in 25 bacterial and archaeal genera isolated from various arsenic-rich environments, most of which belong to the Alpha-, Beta-, or Gammaproteobacteria phylum (7,10,12,14,23,25,29,32,37). Recent studies based on environmental DNA extracted from soils, sediments, a...

Natural Hot Spots for Gain of Multiple Resistances: Arsenic and Antibiotic Resistances in Heterotrophic, Aerobic Bacteria from Marine Hydrothermal Vent Fields

“…This suggests that ACR3 was mostly vertically inherited from the gene pool of the respective taxonomic clade and, therefore, absent from mobile genetic elements and also indicates an ancient origin of the enzyme (29,37). However, one strain, E. citreus As(V) 16, showed putative horizontal gene transfer (HGT) events with ACR3, suggesting that HGT also played a role during the inheritance process (38,39). A growing body of evidence suggests that nonpathogenic environmental organisms are a reservoir of resistance genes, including genes conferring resistance to antibiotics.…”

Metagenomic analysis revealed highly diverse microbial arsenic metabolism genes in paddy soils with low-arsenic contents

“…The MEGA 5 (Tamura et al, 2011) and PAST (Hammer et al, 2001) local tools were used to construct a phylogenetic tree and perform cluster analysis. BAND program (Heinrich-Salmeron et al, 2011) and MATLAB software (http://www.mathworks.com/) were applied to visualize the As metabolism genes abundance profile.…”

Functions and Unique Diversity of Genes and Microorganisms Involved in Arsenite Oxidation from the Tailings of a Realgar Mine

“…To detect the diversity of the arsenite oxidases in microbial communities from the tailings of the Shimen realgar mine, three pairs of primers were used to amplify the aioA genes from the metagenomic DNA of the samples as described previously (Table 1) (33,48). PCR products were gel purified using the E.Z.N.A.…”

“…Until now, the aioA genes have been identified from more than 80 genera of bacteria and archaebacteria, which were isolated from various arsenic-contaminated environments. Most of the aioA genes belong to Alphaproteobacteria, Betaproteobacteria, or Gammaproteobacteria (31)(32)(33)(34)36). However, little is known about the microbial diversity and functional features of AOB from the tailings of a realgar mine that are characteristic of high concentrations of arsenic and sulfate.…”

“…The aioA gene is usually used as a valuable molecular marker for investigations of the diversity, evolution, and potential activity of AOB (22,29). Recent studies based on metagenomic DNA extracted from soils, sediments, water, minerals, tailings, and geothermal mats with different chemical characteristics and various levels of arsenic contamination suggested that the diversities of AioA proteins differ considerably among these sampling sites (29)(30)(31)(32)(33)(34)(35)(36)(37). Until now, the aioA genes have been identified from more than 80 genera of bacteria and archaebacteria, which were isolated from various arsenic-contaminated environments.…”