Impact of arsenic on microbial community structure and their metabolic potential from rice soils of West Bengal, India

Abstract

Paddy soil is a heterogenous ecosystem that harbours diverse microbial communities critical for maintaining ecosystem sustainability and crop yield. Considering the importance of soil in crop production and recent reports on its contamination with arsenic (As) across the South East Asia, its microbial community composition and biogeochemical functions remained inadequately studied. We have characterized the microbial communities of rice soil from eleven paddy fields of As-contaminated sites from West Bengal (India), through metagenomics and amplicon sequencing. 16S rRNA gene sequencing showed considerable bacterial diversity [over 0.2 million Operational Taxonomic Units (OTUs)] and abundance (upto 1.6 × 10⁷ gene copies/g soil). Existence of a core-microbiome (261 OTUs conserved out of a total 141,172 OTUs) across the samples was noted. Most of the core-microbiome members were also found to represent the abundant taxa of the soil. Statistical analyses suggested that the microbial communities were highly constrained by As, Fe K, N, PO₄^3-, SO₄^2- and organic carbon (OC). Members of Proteobacteria, Actinobacteria, Acidobacteria, Chloroflexi, Planctomycetes and Thaumarchaeota constituted the core-microbiome. Co-occurrence network analysis displayed significant interaction among diverse anaerobic, SO₄^2- and NO₃^- reducing, cellulose and other organic matter or C1 compound utilizing, fermentative and aerobic/facultative anaerobic bacteria and archaea. Correlation analysis suggested that taxa which were positively linked with soil parameters that maintain soil health and productivity (e.g., N, K, PO₄^3- and Fe) were adversely impacted by increasing As concentration. Shotgun metagenomics highlighted major metabolic pathways controlling the C (3-hydroxypropionate bicycle), N (Denitrification, dissimilatory NO₃^- reduction to ammonium), and S (assimilatory SO₄^2- reduction and sulfide oxidation) cycling, As homeostasis (methylation and reduction) and plant growth promotion (polyphosphate hydrolysis and auxin biosynthesis). All these major biogeochemical processes were found to be catalyzed by the members of most abundant/core-community.

Keywords: Arsenic; Co-occurrence network; Core-community; Paddy soil; Rice; Soil health; Soil microbiome.