Coupled Aerobic Methane Oxidation and Arsenate Reduction Contributes to Soil-Arsenic Mobilization in Agricultural Fields

Abstract

Microbial oxidation of organic compounds can promote arsenic release by reducing soil-associated arsenate to the more mobile form arsenite. While anaerobic oxidation of methane has been demonstrated to reduce arsenate, it remains elusive whether and to what extent aerobic methane oxidation (aeMO) can contribute to reductive arsenic mobilization. To fill this knowledge gap, we performed incubations of both microbial laboratory cultures and soil samples from arsenic-contaminated agricultural fields in China. Incubations with laboratory cultures showed that aeMO could couple to arsenate reduction, wherein the former bioprocess was carried out by aerobic methanotrophs and the latter by a non-methanotrophic bacterium belonging to a novel and uncultivated representative of Burkholderiaceae. Metagenomic analyses combined with metabolite measurements suggested that formate served as the interspecies electron carrier linking aeMO to arsenate reduction. Such coupled bioprocesses also take place in the real world, supported by a similar stoichiometry and gene activity in the incubations with natural paddy soils, and contribute up to 76.2% of soil-arsenic mobilization into pore waters in the top layer of the soils where oxygen was present. Overall, this study reveals a previously overlooked yet significant contribution of aeMO to reductive arsenic mobilization.

A Case Study: Arsenic, Cadmium and Copper Distribution in the Soil–Rice System in Two Main Rice-Producing Provinces in China

“…In recent decades, progress has been achieved to understand the geochemical cycling and translocation of As and Cd from soil to plants [34][35][36]. Environmental factors influencing HM bioavailability in the soil include pH, redox state (Eh), ECE, P, OM, salinity, microbial activity and other components, as shown in Table 1 [37][38][39]. The process of activation and dissolution of As/Cd from the adsorption state on the surface of soil particles and migration to the rice root surface is crucial to determining their bioavailability.…”

Unexpected genetic and microbial diversity for arsenic cycling in deep sea cold seep sediments

“…So far, As-transforming microbes and As-related genes have been widely investigated in various natural environments, including polluted and pristine soils 27 , 28 , terrestrial geothermal springs 29 – 31 , wetlands 32 , 33 , pelagic oxygen-deficient zones 34 , groundwater 35 , etc. For example, metagenomic and metatranscriptomic analyses revealed that Aquificae were the key players for the arsC -based detoxification in Tengchong geothermal springs 29 .…”

Unexpected genetic and microbial diversity for arsenic cycling in deep sea cold seep sediments

“…So far, As-transforming microbes and As-related genes have been widely investigated in various natural environments, including polluted and pristine soils 27,28 , terrestrial geothermal springs [29][30][31] , wetlands 32,33 , pelagic oxygen-deficient zones 34 , groundwater 35 , etc. For example, metagenomic and metatranscriptomic analyses revealed that Aquificae are the key players for the arsC-based detoxification in Tengchong geothermal springs 29 .…”