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Release of arsenic from soil by a novel dissimilatory arsenate-reducing bacterium, Anaeromyxobacter sp. strain PSR-1.

ABSTRACT: A novel arsenate-reducing bacterium, designated strain PSR-1, was isolated from arsenic-contaminated soil. Strain PSR-1 was phylogenetically closely related to Anaeromyxobacter dehalogenans 2CP-1(T) with 16S rRNA gene similarity of 99.7% and coupled the oxidation of acetate with the reduction of arsenate. Arsenate reduction was inhibited almost completely by respiratory inhibitors such as dicumarol and 2-heptyl-4-hydroxyquinoline N-oxide. Strain PSR-1 also utilized soluble Fe(III), ferrihydrite, nitrate, oxygen, and fumarate as electron acceptors. Strain PSR-1 catalyzed the release of arsenic from arsenate-adsorbed ferrihydrite. In addition, inoculation of washed cells of strain PSR-1 into sterilized soil successfully reproduced arsenic release. Arsenic K-edge X-ray absorption near-edge structure (XANES) analysis revealed that the proportion of arsenite in the soil solid phase actually increased from 20% to 50% during incubation with washed cells of strain PSR-1. These results suggest that strain PSR-1 is capable of reducing not only dissolved arsenate but also arsenate adsorbed on the soil mineral phase. Arsenate reduction by strain PSR-1 expands the metabolic versatility of Anaeromyxobacter dehalogenans. Considering its distribution throughout diverse soils and anoxic sediments, Anaeromyxobacter dehalogenans may play a role in arsenic release from these environments.

SUBMITTER: Kudo K

PROVIDER: S-EPMC3719522 | biostudies-literature | 2013 Aug

REPOSITORIES: biostudies-literature

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Release of arsenic from soil by a novel dissimilatory arsenate-reducing bacterium, Anaeromyxobacter sp. strain PSR-1.

Kudo Keitaro K Yamaguchi Noriko N Makino Tomoyuki T Ohtsuka Toshihiko T Kimura Kenta K Dong Dian Tao DT Amachi Seigo S

Applied and environmental microbiology 20130524 15

A novel arsenate-reducing bacterium, designated strain PSR-1, was isolated from arsenic-contaminated soil. Strain PSR-1 was phylogenetically closely related to Anaeromyxobacter dehalogenans 2CP-1(T) with 16S rRNA gene similarity of 99.7% and coupled the oxidation of acetate with the reduction of arsenate. Arsenate reduction was inhibited almost completely by respiratory inhibitors such as dicumarol and 2-heptyl-4-hydroxyquinoline N-oxide. Strain PSR-1 also utilized soluble Fe(III), ferrihydrite, ...[more]

PMID: 23709511

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Project description:Anaeromyxobacter sp. strain PSR-1, a dissimilatory arsenate [As(V)]-reducing bacterium, can utilize As(V) as a terminal electron acceptor for anaerobic respiration. A previous draft genome analysis revealed that strain PSR-1 lacks typical respiratory As(V) reductase genes (arrAB), which suggested the involvement of another protein in As(V) respiration. Dissimilatory As(V) reductase activity of strain PSR-1 was induced under As(V)-respiring conditions and was localized predominantly in the periplasmic fraction. The activity was visualized by partially denaturing gel electrophoresis, and liquid chromatography-tandem mass spectrometry analysis identified proteins involved in the active band. Among these proteins, a protein annotated as molybdopterin-dependent oxidoreductase (PSR1_00330) exhibited the highest sequence coverage, 76%. Phylogenetic analysis revealed that this protein was a homolog of tetrathionate reductase catalytic subunit TtrA. However, the crude extract of strain PSR-1 did not show significant tetrathionate reductase enzyme activity. Comparative proteomic analysis revealed that the protein PSR1_00330 and a homolog of tetrathionate reductase electron transfer subunit TtrB (PSR1_00329) were expressed abundantly and specifically under As(V)-respiring conditions, respectively. The genes encoding PSR1_00330 and PSR1_00329 formed an operon-like structure along with a gene encoding a c-type cytochrome (cyt c), and their transcription was upregulated under As(V)-respiring conditions. These results suggest that the protein PSR1_00330, which lacks tetrathionate reductase activity, functions as a dissimilatory As(V) reductase in strain PSR-1. Considering the wide distribution of TtrA homologs among bacteria and archaea, they may play a hitherto unknown role along with conventional respiratory As(V) reductase (Arr) in the biogeochemical cycling of arsenic in nature.IMPORTANCE Dissimilatory As(V)-reducing prokaryotes play significant roles in arsenic release and contamination in groundwater and threaten the health of people worldwide. Generally, such prokaryotes reduce As(V) by means of a respiratory As(V) reductase designated Arr. However, some dissimilatory As(V)-reducing prokaryotes such as Anaeromyxobacter sp. strain PSR-1 lack genes encoding Arr, suggesting the involvement of other protein in As(V) reduction. In this study, using multiple proteomic and transcriptional analyses, it was found that the dissimilatory As(V) reductase of strain PSR-1 was a protein closely related to the tetrathionate reductase catalytic subunit (TtrA). Tetrathionate reductase is known to play a role in anaerobic respiration of Salmonella on tetrathionate, but strain PSR-1 showed neither growth on tetrathionate nor significant tetrathionate reductase enzyme activity. These results suggest the possibility that TtrA homologs encoded in a wide variety of archaeal and bacterial genomes might function as dissimilatory As(V) reductases.

Project description:The reduction of arsenate [As(V)] to arsenite [As(III)] by dissimilatory As(V)-reducing bacteria, such as Geobacter spp., may play a significant role in arsenic release from anaerobic sediments into groundwater. The biochemical and molecular mechanisms by which these bacteria cope with this toxic element remain unclear. In this study, the expression of several genes involved in arsenic respiration (arr) and resistance (ars) was determined using Geobacter sp. strain OR-1, the only cultured Geobacter strain capable of As(V) respiration. In addition, proteins expressed differentially under As(V)-respiring conditions were identified by semiquantitative proteomic analysis. Dissimilatory As(V) reductase (Arr) of strain OR-1 was localized predominantly in the periplasmic space, and the transcription of its gene (arrA) was upregulated under As(V)-respiring conditions. The transcription of the detoxifying As(V) reductase gene (arsC) was also upregulated, but its induction required 500 times higher concentration of As(III) (500 μM) than did the arrA gene. Comparative proteomic analysis revealed that in addition to the Arr and Ars proteins, proteins involved in the following processes were upregulated under As(V)-respiring conditions: (i) protein folding and assembly for rescue of proteins with oxidative damage, (ii) DNA replication and repair for restoration of DNA breaks, (iii) anaplerosis and gluconeogenesis for sustainable energy production and biomass formation, and (iv) protein and nucleotide synthesis for the replacement of damaged proteins and nucleotides. These results suggest that strain OR-1 copes with arsenic stress by orchestrating pleiotropic processes that enable this bacterium to resist and actively metabolize arsenic.IMPORTANCE Dissimilatory As(V)-reducing bacteria, such as Geobacter spp., play significant roles in arsenic release and contamination in groundwater and threaten the health of people worldwide. However, the biochemical and molecular mechanisms by which these bacteria cope with arsenic toxicity remain unclear. In this study, it was found that both respiratory and detoxifying As(V) reductases of a dissimilatory As(V)-reducing bacterium, Geobacter sp. strain OR-1, were upregulated under As(V)-respiring conditions. In addition, various proteins expressed specifically or more abundantly in strain OR-1 under arsenic stress were identified. Strain OR-1 actively metabolizes arsenic while orchestrating various metabolic processes that repair oxidative damage caused by arsenic. Such information is useful in assessing and identifying possible countermeasures for the prevention of microbial arsenic release in nature.

Project description:Reductive transformation of toxic arsenic (As) species by As reducing bacteria (AsRB) is a key process in As-biogeochemical-cycling within the subsurface aquifer environment. In this study, we have characterized a Gram-stain-negative, non-spore-forming, rod-shaped As reducing bacterium designated KAs 5-3T, isolated from highly As-contaminated groundwater of India. Strain KAs 5-3T displayed high 16S rRNA gene sequence similarity to the members of the genus Pseudoxanthomonas, with P. mexicana AMX 26BT (99.25% similarity), P. japonensis 12-3T (98.9 0%), P. putridarboris WD-12T (98.02%), and P. indica P15T (97.27%) as closest phylogenetic neighbours. DNA-DNA hybridization study unambiguously indicated that strain KAs 5-3T represented a novel species that was separate from reference strains of P. mexicana AMX 26BT (35.7%), P. japonensis 12-3T (35.5%), P. suwonensis 4M1T (35.5%), P. wuyuanensis XC21-2T (35.0%), P. indica P15T (32.5%), P. daejeonensis TR6-08T (32.0%), and P. putridarboris WD12T (22.1%). The DNA G+C content of strain KAs 5-3T was 64.9 mol %. The predominant fatty acids were C15:0 (37.4%), C16:0 iso (12.6%), C17:1 iso ω9c (10.5%), C15:0 anteiso (9.5%), C11:0 iso 3-OH (8.5%), and C16:1 ω7c/ C16:1 ω6c (7.5%). The major polar lipids were diphosphatidylglycerol, phosphatidyldimethylethanolamine, phosphatidylcholine, and two unknown phospholipids (PL1, PL2). Ubiquinone 8 (Q8) was the predominant respiratory quinone and spermidine was the major polyamine of the strain KAs 5-3T. Cells of strain KAs 5-3T showed the ability to use O2, As5+, NO3-, NO2-, and Fe3+ as terminal electron acceptors as well as to reduce As5+ through the cytosolic process under aerobic incubations. Genes encoding arsenate reductase (arsC) for As-detoxification, nitrate- and nitrite reductase (narG and nirS) for denitrification were detected in the strain KAs 5-3T. Based on taxonomic and physiological data, strain KAs 5-3T is described as a new representative member of the genus Pseudoxanthomonas, for which the name Pseudoxanthomonas arseniciresistens sp. nov. is proposed. The type strain is KAs 5-3T (= LMG 29169T = MTCC 12116T = MCC 3121T).

Dataset Information

Release of arsenic from soil by a novel dissimilatory arsenate-reducing bacterium, Anaeromyxobacter sp. strain PSR-1.

Publications

Release of arsenic from soil by a novel dissimilatory arsenate-reducing bacterium, Anaeromyxobacter sp. strain PSR-1.

Similar Datasets

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