Metagenomic analysis displays the potential predictive biodegradation pathways of the persistent pesticides in agricultural soil with a long record of pesticide usage

Abstract

Microbes are crucial in removing various xenobiotics, including pesticides, from the environment, specifically by mineralizing these hazardous pollutants. However, the specific procedure of microbe-mediated pesticide degradation and its consequence on the environment remain elusive owing to limitations in culturing techniques. Therefore, in this study, we have investigated i) the physicochemical and elemental compositions of PCAS (pesticide-contaminated agricultural soils) and NS (natural soils); ii) the bacterial communities and degradation pathways, as well as some novel biodegradation genes (BDGs) and pesticide degradation genes (PDGs) across two different landscapes (PCAS and NS) by applying high-throughput sequencing. The chemical and elemental composition analyses showed that all nutrients (P, K, N, S, Mn, B, and Zn) were significantly higher in PCAS than in NS (p ≤ 0.05). The results of the 16S rRNA amplicon sequencing analysis of pesticide-contaminated (PCAS-1, PCAS-2, PCAS-3, PCAS-4) samples showed that the relative abundance of the phylum Proteobacteria (30-36%) > Actinobacteria (15-20%) > Firmicutes (13-14%) > Bacteroidetes (7-13%), were higher compared to the natural soil (NS-1, NS2). Consistent with this, a phylogenetic shift was observed with (alpha, beta, and gamma Proteobacteria) being abundant in PCAS, whereas delta and epsilon groups were more prevalent in NS. The functional characterization of the PCAS and NS by PICRUSt2 revealed that bacterial communities play a significant role in pesticide metabolism. Predictive metagenome analysis of contaminated soils showed the role of core degrading genes in membrane transport, stress response, regulatory genes, resource transport, and environmental sensing. Furthermore, 14 BDGs and 30 PDGs were examined, with a relative abundance of 0.081−1.029 % and 0.107–0.8903 % in each PCAS, respectively. The major BDGs and PDGs, with the compounds they hydrolyze, include ppo (polyphenol oxidase and laccase), CYP (cytochrome p450 protein), lip gene (lignin peroxidase), similarly, among the PDGs mhel (carbendazim), opd (organophosphate), mpd (methyl parathion), atzA, atzB, atzD, atzF and trzN (atrazine), chd (chlorothalonil), hdx (metamitron), hdl-1 (isoproturon) and fmo (nicosulfuron). Overall, our findings demonstrated the significance of utilizing metagenomic methods to predict microbial aided degradation in the ecology of contaminated environments.