Diversity and Abundance of Arsenic Biotransformation Genes in Paddy Soils from Southern China

Abstract

Microbe-mediated arsenic (As) biotransformation in paddy soils determines the fate of As in soils and its availability to rice plants, yet little is known about the microbial communities involved in As biotransformation. Here, we revealed wide distribution, high diversity, and abundance of arsenite (As(III)) oxidase genes (aioA), respiratory arsenate (As(V)) reductase genes (arrA), As(V) reductase genes (arsC), and As(III) Sadenosylmethionine methyltransferase genes (arsM) in 13 paddy soils collected across Southern China. Sequences grouped with As biotransformation genes are mainly from rice rhizosphere bacteria, such as some Proteobacteria, Gemmatimonadales, and Firmicutes. A significant correlation of gene abundance between arsC and arsM suggests that the two genes coexist well in the microbial As resistance system. Redundancy analysis (RDA) indicated that soil pH, EC, total C, N, As, and Fe, C/N ratio, SO 4 2− -S, NO 3 − -N, and NH 4 + -N were the key factors driving diverse microbial community compositions. This study for the first time provides an overall picture of microbial communities involved in As biotransformation in paddy soils, and considering the wide distribution of paddy fields in the world, it also provides insights into the critical role of paddy fields in the As biogeochemical cycle. ■ INTRODUCTIONChina is the world's largest rice producer, accounting for about 30% of the total world production (http://beta.irri.org/ statistics), mostly in Southern China.1 As a highly toxic metalloid, arsenic (As) contamination in paddy fields has emerged as a serious health concern worldwide, 2 especially considering that the anaerobic conditions in paddy soils are conducive to As mobilization, 3,4 resulting in a markedly enhanced bioavailability of As to rice plants. 5 It is now recognized that consumption of rice constitutes a large proportion of the dietary intake of As for the populations in China and other Asian countries. 6−8 Microbes are the key drivers for As biotransformation in paddy soils, catalyzing arsenate (As(V)) reduction, arsenite (As(III)) oxidation and methylation.9 Microcosm studies have demonstrated that microbes capable of As reduction, oxidation, and methylation often coexist in paddy soils, and their relative abundance and activity determine the fate of As in the paddy environment and the bioavailability of As to plants. 10−12 There are two known microbial pathways for As(V) reduction, the respiratory pathway mediated by arrA genes 13 and the detoxification pathway mediated by arsC genes.14 As(III) oxidation is catalyzed by As(III) oxidases, which are encoded by aioA and aioB genes for the two subunits of the enzyme 15 and have been identified in several heterotrophic and chemoautotrophic microorganisms. 16 Moreover, As(III) can be methylated by microbes into various organic As species. 17Arsenic biomethylation is catalyzed by As(III) S-adenosylmethionine methyltransferase (ArsM), which is encoded by arsM genes.18

Metagenomic analysis revealed highly diverse microbial arsenic metabolism genes in paddy soils with low-arsenic contents

“…As(III) methylation genes (arsM) constituted secondary important part of total As metabolism genes (6e9%) among all five paddy soils, and higher than aio and arr in our samples, implying a strong potential to produce methylated As species, which could be uptake by rice roots and explain why most rice contains unusually high concentrations of methylated As species compared with other cereals (Jia et al, 2013). The low abundance of arr genes compared with the others detected in the five paddy soils, which has also been confirmed either in paddy soils or As and antimony (Sb) contaminated mine field (Jia et al, 2014(Jia et al, , 2013Luo et al, 2014;Zhang et al, 2015), could be partly ascribed to their specific presence in anaerobic As(V) respiring bacteria (Malasarn et al, 2004;Silver and Phung, 2005). Previous studies showed that total As concentrations in paddy soils correlated positively with the abundance of genes involved in As biotransformation processes (Zhang et al, 2015), and concentrations of different As species in soil solutions have also been revealed good correlations with the abundance of genes responsible for different As biotransformation processes in microcosm experiments (Jia et al, 2014(Jia et al, , 2013.…”

“…The low abundance of arr genes compared with the others detected in the five paddy soils, which has also been confirmed either in paddy soils or As and antimony (Sb) contaminated mine field (Jia et al, 2014(Jia et al, , 2013Luo et al, 2014;Zhang et al, 2015), could be partly ascribed to their specific presence in anaerobic As(V) respiring bacteria (Malasarn et al, 2004;Silver and Phung, 2005). Previous studies showed that total As concentrations in paddy soils correlated positively with the abundance of genes involved in As biotransformation processes (Zhang et al, 2015), and concentrations of different As species in soil solutions have also been revealed good correlations with the abundance of genes responsible for different As biotransformation processes in microcosm experiments (Jia et al, 2014(Jia et al, , 2013. Our results showed no significant correlation between total As content and abundance of different types of As metabolism genes (Table S1), which were possibly due to the low As level in these soil samples.…”

“…3). Zhang et al (2015) also revealed the strong correlation of arsC and arsM gene copies based on quantitative PCR, and suggested that similar compositions of microbial communities are involved in As(V) detoxification reduction and As(III) methylation in paddy soil. Considering that ars, aio, and arsM genes are separately involved in cytoplasmic As(V) reduction, As(III) oxidation, and As(III) methylation processes, the significant correlation between the abundances of ars, aio, and arsM gene indicated the co-existence and close-relation of these different As resistance systems in microbes in paddy soil (Jia et al, 2014(Jia et al, , 2013Zhang et al, 2015;Zhu et al, 2014).…”

“…Arsenic (As) is a notoriously poisonous trace element which is ubiquitous in natural environment and can enter into the food chain through various pathways (Cai et al, 2013;Xiao et al, 2012;Zhang et al, 2015;Zhu et al, 2014). Typically, rice can accumulate As from both polluted and unpolluted paddy soils, posing a potential health risk to populations with high rice consumption in China, Southern Asian and certain Latin American areas (Li et al, 2011;Zhu et al, 2014).…”

Arsenic Transformation in Swine Wastewater with Low-Arsenic Content during Anaerobic Digestion

“…The arsC, aioA, arsM and 16S rRNA gene copy numbers were measured through qPCR analysis. The qPCR thermocycling conditions for 16S rRNA gene and As metabolism genes were described elsewhere [12].…”