Viral involvement in microbial anaerobic methane oxidation-mediated arsenic mobilization in paddy soil

Youjing Wang; Di Tong; Haodan Yu; Yujie Zhou; Caixian Tang; Randy A Dahlgren; Jianming Xu

doi:10.1016/j.jhazmat.2024.136758

Viral involvement in microbial anaerobic methane oxidation-mediated arsenic mobilization in paddy soil

J Hazard Mater. 2024 Dec 3:484:136758. doi: 10.1016/j.jhazmat.2024.136758. Online ahead of print.

Authors

Youjing Wang¹, Di Tong¹, Haodan Yu¹, Yujie Zhou¹, Caixian Tang², Randy A Dahlgren³, Jianming Xu⁴

Affiliations

¹ Institute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou 310058, China; Zhejiang Provincial Key Laboratory of Agricultural Resources and Environment, Zhejiang University, Hangzhou 310058, China.
² La Trobe Institute for Sustainable Agriculture and Food, Department of Animal, Plant & Soil Sciences, La Trobe University, Bundoora, VIC 3086, Australia.
³ Department of Land, Air and Water Resources, University of California, Davis, CA 95616, USA.
⁴ Institute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou 310058, China; Zhejiang Provincial Key Laboratory of Agricultural Resources and Environment, Zhejiang University, Hangzhou 310058, China. Electronic address: jmxu@zju.edu.cn.

PMID: 39644851
DOI: 10.1016/j.jhazmat.2024.136758

Abstract

Anaerobic oxidation of methane (AOM) facilitates arsenic (As) mobilization, posing a significant environmental risk. Soil viruses potentially participate in the microbial AOM process, yet their roles in methane-mediated As mobilization of paddy soil remain elusive. Here, an anaerobic microcosm study was conducted by inoculating microbial suspension with extracellular free virus and mitomycin C (MC)-induced virus, along with ¹³CH₄ injection. The results showed that extracellular free virus enhanced while MC-induced virus suppressed ¹³CH₄-mediated As mobilization. During the AOM process, both viruses inhibited ¹³CH₄ oxidation to ¹³CO₂. However, the extracellular free virus suppressed whereas the MC-induced virus enhanced ¹³CH₄ consumption, likely attributed to the viral influence on the ANME-2d abundance. The methane consumption differences were inferred to influence As reduction, as evidenced by a strong correlation between As(III) and ¹³CH₄ consumption concentrations. Moreover, virus-mediated methane assimilation into microbial biomass carbon influenced the overall microbial population. An increased abundance of Geobacter in the extracellular free virus treatment elevated net As(III) concentrations (up to 260 %) relative to treatment without virus in the presence of ¹³CH₄. In contrast, MC-induced virus led to a net 122 % reduction in As(III) concentration due to decreased Geobacter abundance. These findings provide new insights into soil viruses in microbial AOM-driven As mobilization, highlighting their crucial functions in soil ecosystems.

Keywords: ANME-2d; Extracellular free virus; MC-induced virus; Methane assimilation; Methane consumption.