Coupled anaerobic methane oxidation and reductive arsenic mobilization in wetland soils

Abstract

Anaerobic methane oxidation is coupled to the reduction of electron acceptors, such as sulfate, and contributes to their biogeochemical cycling in the environment. However, whether arsenate acts as an alternative electron acceptor of anaerobic methane oxidation and how this influences global arsenic transformations remains elusive. Here, we present incubations of arsenate-contaminated wetland soils from seven provinces in China. Using isotopically labelled methane, we find that anaerobic methane oxidation was linked to arsenate reduction at a rate approaching the theoretical arsenic/methane stoichiometric ratio of 4. In microcosm incubations with natural wetland soils, we find that the coupled pathway of anaerobic methane oxidation and arsenate reduction contributed 26 to 49% of total arsenic release from soils, with arsenic in the more soluble and toxic form arsenite. Comparative gene quantification and metagenomic sequencing suggest that the coupled pathway was facilitated by anaerobic methanotrophs, either independently or synergistically with arsenate-reducing bacteria through reverse methanogenesis and respiratory arsenate reduction. Further bioinformatic analyses show that genes coding for reverse methanogenesis and respiratory arsenate reduction are universally co-distributed in nature. This suggests that coupling of anaerobic methane oxidation and arsenate reduction is a potentially global but previously overlooked process, with implications for arsenic mobilization and environmental contamination.

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Fig. 1: Geographic map of field-sampling locations.
Fig. 2: Stoichiometry and correlation of As(V) and 13C-DIC concentrations in experiments inoculated by soil samples.
Fig. 3: Phylogeny of mcrA based on amino acid sequences.
Fig. 4: Phylogeny of DMSOR superfamily based on amino acid sequences.
Fig. 5: Increased dissolved arsenic and gaseous 13CO2 of microcosm incubations using representative soils.
Fig. 6: Global map with environmental samples containing both ANME-mcrA and arrA on the basis of bioinformatic prediction.

Data availability

All the metagenomic sequencing data have been submitted to the Sequence Read Archive, with BioProject accession number of PRJNA612595. The source data have been deposited into the Open Science Framework (OSF) at https://doi.org/10.17605/OSF.IO/N4SEF. Source data are provided with this paper.

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Acknowledgements

The authors greatly thank the National Natural Science Foundation of China (grants 51878596, 41991332 and 21577123), the Natural Science Funds for Distinguished Young Scholar of Zhejiang Province (LR17B070001) and the National Key Technology R&D Program (2018YFC1802203) for their financial support.

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Contributions

L.-D.S. conceived and conducted the incubations with soil inocula, performed and analysed metagenomics and other bioinformatics, evaluated and arranged the results, and drafted the manuscript; T.G. took natural samples, measured physicochemical characteristics and quantified the functional genes/transcripts; P.-L.L. and Z.-F.N. helped perform the experiments inoculated by soil samples and microcosm incubations; Y.-J.Z. performed the microcosm incubations; X.-J.T. supervised the project, conceived the experiments and wrote the manuscript; P.Z., L.-Z.Z., Y.-G.Z. and A.K. assisted in design and set-up of the project and contributed to the manuscript preparation; H.-P.Z. initiated and supervised the project, conceived the experiments and wrote the manuscript; all authors contributed to revising the manuscript.

Corresponding authors

Correspondence to Xian-Jin Tang or He-Ping Zhao.

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The authors declare no competing interests.

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Peer review information Primary Handling Editors: Clare Davis; Xujia Jiang.

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Extended data

Extended Data Fig. 1 Reduced As(V) and produced 13DIC of experiments inoculated by soil samples during the whole incubation (7 days).

The main differences between these two groups are 13CH4 (top comparison) and As(V) (bottom comparison), respectively. Error bars indicate standard deviations of triplicate setups. The value of ΔAs(III)/ΔAs(V) represents the ratio of increased dissolved As(III) to decreased dissolved As(V). Asterisks indicate the statistical significance of the difference between experiment setups and corresponding control setups calculated by Kruskal-Wallis test.

Extended Data Fig. 2 Stoichiometry and kinetics of AOM-AsR for the AH-MAS-1 soil sample.

Mass balance was tested for 13CH4 (a) and As(V) (b). Electron balance between 13CH4 oxidation and As(V) reduction was studied in terms of rate (c) and ratio (d). Error bars indicate standard deviations of triplicate setups. The confidence levels for fitting curves are 95%. Please note the different y-axis scales for different items.

Extended Data Fig. 3 Gene abundance and correlation with methane oxidation and arsenate reduction rates.

Absolute abundances of mcrA and arrA (copies/g dry soil) were normalized by logarithm with a base of ten (a). Gene abundances and reaction rates were correlated using Spearman rank correlation (b and c), where ρ and p indicate the correlation efficiency and statistic probability, respectively. Error bars indicate standard deviations of triplicates. The points (SC-MY-1, YN-KM, and AH-MAS-1) in the grey circle (c) of which standard residual is 2-fold more than the standard deviation are removed based on Casewise Diagnostics. Their relatively high ATL values might explain why As(V) could be reduced rapidly at low arrA abundances (Supplementary Fig. 4).

Extended Data Fig. 4 Detailed phylogeny of respiratory arsenate reductase.

The proteins recovered in this study are highlighted in purple. Bootstrap values are generated from 100 replicates. The scale bar represents amino acid changes.

Extended Data Fig. 5 Phylogeny of respiratory arsenate reductase beta subunit (ArrB) and closely related anaerobic arsenite oxidase beta subunit (ArxB).

The proteins recovered in this study are highlighted in purple. A 4Fe-4S ferredoxin is used as the outgroup. Bootstrap values are generated from 100 replicates. The scale bar represents amino acid changes.

Extended Data Fig. 6 Putative metabolic pathways of AOM-AsR.

Methanoperedenaceae members perform AOM-AsR independently using arsenate reductase acquired through lateral gene transfer (a). Electrons are generated from methane oxidation via the reverse methanogenesis pathway in ANME groups, and then transferred to arsenate reducers possibly through multi-haem cytochromes (b). Abbreviations: Mcr, methyl-coenzyme M reductase; MHC, multi-haem cytochrome; Arr, respiratory arsenate reductase.

Extended Data Fig. 7 Contents of 13CO2 in the headspace in the microcosm incubations.

(a), (c), and (e) are incubated with YN-MG-2, SC-CD-1, and SC-MY-2, respectively, while (b), (d), and (f) use the corresponding autoclaved samples. The dark and light grey in each figure indicate the experimental setups amended with environmentally relevant concentrations of 13CH4, and the control setups without methane addition, respectively. The probability (i.e. p-values) of the differences between two setups was calculated using Kruskal-Wallis test. Error bars indicate standard deviations of triplicate setups.

Extended Data Fig. 8 Concentrations of As(V) and As(III) in the porewaters in the microcosm incubations.

(a), (c), and (e) were incubated with YN-MG-2, SC-CD-1, and SC-MY-2, respectively, while (b), (d), and (f) show the corresponding autoclaved samples. The dark and light red in each figure indicate the experimental setups amended with environmentally relevant concentrations of 13CH4, and the control setups without methane addition, respectively. The upper parts show As(III) while the bottom ones show As(V). Please note the different y-axis scales in the different panels. The probability (i.e. p-values) of differences between two setups was calculated using Kruskal-Wallis test. Error bars indicate standard deviations of triplicate setups.

Extended Data Fig. 9 Concentrations of total Fe and Fe(II) in the porewaters in the microcosm incubations.

(a), (c), and (e) were incubated with YN-MG-2, SC-CD-1, and SC-MY-2, respectively, while (b), (d), and (f) used the corresponding autoclaved samples. The dark and light pink in each figure indicate the experimental setups amended with environmentally relevant concentrations of 13CH4, and the control setups without methane addition, respectively. The upper parts show total Fe while the bottom ones show Fe(II). Please note the different y-axis scales in the different panels. The probability (i.e. p-values) of differences between two setups was calculated using Kruskal-Wallis test. Error bars indicate standard deviations of triplicate setups.

Extended Data Fig. 10 Concentrations of total Mn in the porewaters during the microcosm incubations.

(a), (c), and (e) were incubated with YN-MG-2, SC-CD-1, and SC-MY-2, respectively, while (b), (d), and (f) used the corresponding autoclaved samples. The dark and light green in each figure indicate the experimental setups amended with environmentally relevant concentrations of 13CH4, and the control setups without methane addition, respectively. The probability (i.e. p-values) of differences between two setups was calculated using Kruskal-Wallis test. Error bars indicate standard deviations of triplicate setups.

Supplementary information

Supplementary Information

Supplementary Discussion, Figs. 1–11, Tables 1–4, captions for Supplementary Datasets 1–3 and references for Supplementary Information citations.

Supplementary Dataset 1

Geographical information of collected natural soil samples.

Supplementary Dataset 2

Physicochemical characteristics of collected natural soil samples.

Supplementary Dataset 3

Geographical information of bioinformatic predicted samples.

Source data

Source Data Fig. 2

Numerical data for Fig. 2.

Source Data Fig. 5

Numerical data for Fig. 5.

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Shi, LD., Guo, T., Lv, PL. et al. Coupled anaerobic methane oxidation and reductive arsenic mobilization in wetland soils. Nat. Geosci. 13, 799–805 (2020). https://doi.org/10.1038/s41561-020-00659-z

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