Microbial populations under fluoride stress: a metagenomic exploration from Indian soil

Abstract

Fluoride exposure, even at a low concentration, significantly impairs crop growth and productivity by inhibiting metabolic enzymes and disrupting photosynthesis. Addressing this challenge, microbial de-fluoridation emerges as a vital strategy to improve soil health, enhance crop growth, and ensure agricultural sustainability. This study analyzed topsoil samples (0-0.2 m depth) from rice fields in three blocks of Purulia district, West Bengal-Arsha, Jhalda-I, and Joypur. Fluoride content in the samples ranged from 58.76 ± 0.76 mg/kg to 282.9 ± 4.9 mg/kg (total) and 1.57 ± 0.02 mg/kg to 2.97 ± 0.03 mg/kg (available). The metagenomic analysis of the collected soil samples revealed diverse microbial communities comprising archaea, bacteria, fungi, and viruses, with Actinobacteria (phylum), Hyphomicrobiales (order), and Nocardioidaceae (family) being the dominant prokaryotes. Arsha soil with comparatively low fluoride contamination exhibited the highest microbial diversity (11,891 taxa), followed by Joypur (11,528 taxa) and Jhalda-I (11,358 taxa), with Arsha showing nearly double the unique microbial taxa compared to the other locations. Clusters of orthologous groups of proteins functional analysis identified 60,898 genes in Arsha, 63,403 genes in Jhalda-I, and 73,334 genes in Joypur, while Kyoto encyclopedia of genes and genomes analysis revealed 9,385, 9,104, and 10,633 genes, respectively. Key genes associated with fluoride metabolism-inorganic pyrophosphatase, divalent metal cation transporter mntH, and putative fluoride ion transporter crcB-were abundant across all sites, highlighting the influence of fluoride on microbial community structure. This study provides the first comprehensive report on soil microbial communities in fluoride-rich areas, highlighting the potential of native fluoride-tolerant microbes to mitigate fluoride toxicity in agricultural soils and offer sustainable, microbe-based solutions to fluoride contamination.

Keywords: Bioremediation; Fluoride tolerant bacteria; Fluoride tolerant genes; Metagenomics; Microbial diversity.