Methylation of arsenic by anaerobic microbial consortia isolated from lake sediment

Bright, Doug A.; Brock, Shona C.; Reimer, Kenneth J.; Cullen, William R.; Hewitt, Gary M.; Jafaar, J.

doi:10.1002/aoc.590080416

Cited by 45 publications

(29 citation statements)

References 12 publications

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“…Among several anaerobic As methylating microbes isolated from an As-contaminated lake sediment, sulfur-reducing microbes were found to possess the highest ability to methylate As. 51 The GeoChip assay ( Figure 2) revealed considerable diversity in the arsM sequences present in the six soils studied. Similarly, Jia et al 36 reported that microbes containing arsM genes were phylogenetically diverse in an As-contaminated paddy soil.…”

Section: ■ Discussionmentioning

confidence: 99%

Arsenic Methylation in Soils and Its Relationship with Microbial arsM Abundance and Diversity, and As Speciation in Rice

Zhao

Harris

Jia

et al. 2013

Environ. Sci. Technol.

187

125

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Methylation of arsenic in soil influences its environmental behavior and accumulation by plants, but little is known about the factors affecting As methylation. As speciation was determined in the pore waters of six soils from diverse geographical locations over 54 days of incubation under flooded conditions. The concentration of methylated As (monomethylarsonic acid, MMA, and dimethylarsinic acid, DMA) varied from 0 to 85 μg L −1 (0 − 69% of the total As in pore water). Two Bangladeshi paddy soils contaminated by irrigation of As-laden groundwater produced large concentrations of inorganic As but relatively little methylated As. Two contaminated paddy soils from China produced a transient peak of DMA during the early phase of incubation. Methylated As represented considerable proportions of the total soluble As in the two uncontaminated soils from the UK and U.S. The copy number of the microbial arsenite methyltransferase gene (arsM) correlated positively with soil pH. However, pore-water methylated As correlated negatively with pH or arsM copy number, and positively with dissolved organic C. GeoChip assay revealed considerable arsM diversity among the six soils, with 27−35 out of 66 sequences in the microarray being detected. As speciation in rice plants grown in the soils generally mirrored that in the pore water. The results suggest that methylated As species in plants originated from the soil and As methylation in soil was influenced strongly by the soil conditions. ■ INTRODUCTIONArsenic (As) is a ubiquitous contaminant in the environment originating from both natural and anthropogenic sources. Because its biogeochemical behavior and toxicity vary greatly among different chemical species, it is important to understand how the speciation of As changes in the environment and what drives such changes. A particularly important case is the paddy rice system because it is now recognized that rice is a major source of As in the human diet. 1 The anaerobic conditions in paddy soils are conducive to the mobilization of arsenite, 2,3 which is taken up inadvertently by rice roots through the strong uptake pathway for silicic acid. 4 Rice grain contains both inorganic As (arsenate and arsenite) and organic As (mostly dimethylarsinic acid, DMA; occasionally also trace amounts of monomethylarsonic acid, MMA, and tetramethylarsonium). 5−9 As speciation in rice varies widely among different riceproducing regions. Market-basket surveys show that Asian rice generally is dominated by inorganic As with DMA typically accounting for about 20% of the total As. [5][6][7]10 In contrast, rice produced in the U.S. and Europe is more variable in As speciation with many samples containing more organic than inorganic As. 5,7,8,10 It is possible that that this geographical pattern reflects the relative bioavailability of inorganic versus organic As in different paddy environments. 10 Compared with inorganic As, methylated As species are more easily accumulated in rice grain. 10 Although pentavalent methylated As species are ...

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Section: ■ Discussionmentioning

confidence: 99%

Arsenic Methylation in Soils and Its Relationship with Microbial arsM Abundance and Diversity, and As Speciation in Rice

Zhao

Harris

Jia

et al. 2013

Environ. Sci. Technol.

187

125

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“…Enrichment cultures of anaerobes isolated from an arseniccontaminated lake in the Canadian sub-Arctic region with five selective media showed extensive formation of methylarsenicals (30). Anaerobic oligotrophs were most active, producing a high proportion of dimethylarsinate.…”

Section: Role Of Anaerobic Microorganismsmentioning

confidence: 99%

Microbial Methylation of Metalloids: Arsenic, Antimony, and Bismuth

Bentley

Chasteen

2002

Microbiol Mol Biol Rev

517

316

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A significant 19th century public health problem was that the inhabitants of many houses containing wallpaper decorated with green arsenical pigments experienced illness and death. The problem was caused by certain fungi that grew in the presence of inorganic arsenic to form a toxic, garlic-odored gas. The garlic odor was actually put to use in a very delicate microbiological test for arsenic. In 1933, the gas was shown to be trimethylarsine. It was not until 1971 that arsenic methylation by bacteria was demonstrated. Further research in biomethylation has been facilitated by the development of delicate techniques for the determination of arsenic species. As described in this review, many microorganisms (bacteria, fungi, and yeasts) and animals are now known to biomethylate arsenic, forming both volatile (e.g., methylarsines) and nonvolatile (e.g., methylarsonic acid and dimethylarsinic acid) compounds. The enzymatic mechanisms for this biomethylation are discussed. The microbial conversion of sodium arsenate to trimethylarsine proceeds by alternate reduction and methylation steps, with S-adenosylmethionine as the usual methyl donor. Thiols have important roles in the reductions. In anaerobic bacteria, methylcobalamin may be the donor. The other metalloid elements of the periodic table group 15, antimony and bismuth, also undergo biomethylation to some extent. Trimethylstibine formation by microorganisms is now well established, but this process apparently does not occur in animals. Formation of trimethylbismuth by microorganisms has been reported in a few cases. Microbial methylation plays important roles in the biogeochemical cycling of these metalloid elements and possibly in their detoxification. The wheel has come full circle, and public health considerations are again important

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“…Tentative links have also been drawn between sulfate-reducing bacteria (SRB) and arsenic biomethylation. Bright et al 30 showed that sulfatereducing as well as fermentative and/or methanogenic cultures enriched from lake sediments produced more methylated arsenic than iron-or manganese-reducing cultures. Mikutta and Rothwell 31 showed that 82% of the As in a sulfate-and Asimpacted peat bog was present as organoarsenic species, and Zeng et al 32 showed that the abundance of methylated As in the roots of a ginseng plant increased 263% following soil amendment with sulfate (SO 4 …”

Section: ■ Introductionmentioning

confidence: 99%

Arsenic Methylation Dynamics in a Rice Paddy Soil Anaerobic Enrichment Culture

Reid

Maillard

Bagnoud

et al. 2017

Environ. Sci. Technol.

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Methylated arsenic (As) species represent a significant fraction of the As accumulating in rice grains, and there are geographic patterns in the abundance of methylated arsenic in rice that are not understood. The microorganisms driving As biomethylation in paddy environments, and thus the soil conditions conducive to the accumulation of methylated arsenic, are unknown. We tested the hypothesis that sulfate-reducing bacteria (SRB) are key drivers of arsenic methylation in metabolically versatile mixed anaerobic enrichments from a Mekong Delta paddy soil. We used molybdate and monofluorophosphate as inhibitors of sulfate reduction to evaluate the contribution of SRB to arsenic biomethylation, and developed degenerate primers for the amplification of arsM genes to identify methylating organisms. Enrichment cultures converted 63% of arsenite into methylated products, with dimethylarsinic acid as the major product. While molybdate inhibited As biomethylation, this effect was unrelated to its inhibition of sulfate reduction and instead inhibited the methylation pathway. Based on arsM sequences and the physiological response of cultures to media conditions, we propose that amino acid fermenting organisms are potential drivers of As methylation in the enrichments. The lack of a demethylating capacity may have contributed to the robust methylation efficiencies in this mixed culture.

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Methylation of arsenic by anaerobic microbial consortia isolated from lake sediment

Cited by 45 publications

References 12 publications

Arsenic Methylation in Soils and Its Relationship with Microbial arsM Abundance and Diversity, and As Speciation in Rice

Arsenic Methylation in Soils and Its Relationship with Microbial arsM Abundance and Diversity, and As Speciation in Rice

Microbial Methylation of Metalloids: Arsenic, Antimony, and Bismuth

Arsenic Methylation Dynamics in a Rice Paddy Soil Anaerobic Enrichment Culture

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