Arsenic Uptake by Rice Is Influenced by Microbe-Mediated Arsenic Redox Changes in the Rhizosphere

Abstract

Arsenic (As) uptake by rice is largely determined by As speciation, which is strongly influenced by microbial activities. However, little is known about interactions between root and rhizosphere microbes, particularly on arsenic oxidation and reduction. In this study, two rice cultivars with different radial oxygen loss (ROL) ability were used to investigate the impact of microbially mediated As redox changes in the rhizosphere on As uptake. Results showed that the cultivar with higher ROL (Yangdao) had lower As uptake than that with lower ROL (Nongken). The enhancement of the rhizospheric effect on the abundance of the arsenite (As(III)) oxidase gene (aroA-like) was greater than on the arsenate (As(V)) reductase gene (arsC), and As(V) respiratory reductase gene (arrA), resulting in As oxidation and sequestration in the rhizosphere, particularly for cultivar Yangdao. The community of As(III)-oxidizing bacteria in the rhizosphere was dominated by α-Proteobacteria and β-Proteobacteria and was influenced by rhizospheric effects, rice straw application, growth stage, and cultivar. Application of rice straw into the soil increased As release and accumulation into rice plants. These results highlighted that uptake of As by rice is influenced by microbial processes, especially As oxidation in the rhizosphere, and these processes are influenced by root ROL and organic matter application. ■ INTRODUCTIONArsenic (As) contamination and its health impacts are widespread around the world. 1,2 Large areas of paddy soils are contaminated by As due to irrigation with As-tainted groundwater, mining, and other industrial activities. Rice is particularly efficient in accumulating As, compared with other cereal crops, as a result of its anaerobic growth conditions. 3 This poses potential harm to people through ingestion of rice, especially in Southeast Asia where rice is consumed as the staple food. 4−6 Rhizospheric chemical processes, such as iron oxidation−reduction and iron plaque formation on root surfaces, play an important role in affecting As uptake by rice plants, and they are largely influenced by oxygen release from rice roots. 7,8 The aerated rice rhizosphere and O 2 -releasing root surface are usually coated with iron (Fe) and manganese (Mn) oxides, while As is precipitated with these oxides mainly as arsenate (As(V)). 8,9 In addition to chemical processes, As speciation and mobility in soils, sediments, and natural water systems are mainly driven by microbial transformations. 10−12 Anaerobic bacteria containing the respiratory reductase (ArrA) can use As(V) as the terminal electron acceptor in respiration and conserve energy from this process. 13 Another pathway for microbial As(V) reduction lies in the widespread As detoxification by As(V) reductase (ArsC). 14,15 Arsenite (As(III)) is more weakly bound to most soil minerals than As(V); thus, As(V) reduction results in As release into soil solutions, especially under anaerobic conditions such as paddy soil. 16,17 On the other hand, some heterotrophic as well a...

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“…In paddy soils, As is released into soil solution mainly in the form of arsenite (As(III)), by As-reducing bacteria and by the reductive dissolution of iron oxyhydroxides which reduces the binding sites of As on minerals (Stroud et al 2011;Xu et al 2008). Elevated concentration of As(III) in the soil solution under anaerobic condition provides As sources to rice plants (Roberts et al 2010;Jia et al 2014). Also, rice absorbs As(III) more efficiently than other cereal crops because of its strong silicon uptake pathway which also allows the quick uptake of As(III) (Ma et al 2008;Su et al 2010).…”