Organochlorine contamination enriches virus-encoded metabolism and pesticide degradation associated auxiliary genes in soil microbiomes

Xiaoxuan Zheng,Mingming Sun,Xin Gong,Yong-Guan Zhu,Ville-Petri Friman,Jinfeng Wang,Feng Hu,Jose Luis Balcazar,Yu Shi,Martin T Jahn

doi:10.1038/s41396-022-01188-w

Abstract

Viruses significantly influence local and global biogeochemical cycles and help bacteria to survive in different environments by encoding various auxiliary metabolic genes (AMGs) associated with energy acquisition, stress tolerance and degradation of xenobiotics. Here we studied whether bacterial (dsDNA) virus encoded AMGs are enriched in organochlorine pesticide (OCP) contaminated soil in China and if viral AMGs include genes linked to OCP biodegradation. Using metagenomics, we found that OCP-contaminated soils displayed a lower bacterial, but higher diversity of viruses that harbored a higher relative abundance of AMGs linked to pesticide degradation and metabolism. Furthermore, the diversity and relative abundance of AMGs significantly increased along with the severity of pesticide contamination, and several biodegradation genes were identified bioinformatically in viral metagenomes. Functional assays were conducted to experimentally demonstrate that virus-encoded L-2-haloacid dehalogenase gene (L-DEX) is responsible for the degradation of L-2-haloacid pesticide precursors, improving bacterial growth at sub-inhibitory pesticide concentrations. Taken together, these results demonstrate that virus-encoded AMGs are linked to bacterial metabolism and biodegradation, being more abundant and diverse in soils contaminated with pesticides. Moreover, our findings highlight the importance of virus-encoded accessory genes for bacterial ecology in stressful environments, providing a novel avenue for using viruses in the bioremediation of contaminated soils.

Highlights

As the most abundant biological entities on earth, viruses of bacteria play a critical role in modulating the ecology of microbial communities through lytic infection and lysogenic conversion of their bacterial hosts [1, 2]
Our findings demonstrate that genes linked to both bacterial metabolism and pesticide degradation were enriched in viral metagenomes in OCPcontaminated soils
We found that organochlorine pesticide (OCP)-contaminated soils had distinct bacterial communities, including a higher relative abundance of taxa previously linked to pesticide degradation, such as Paraburkholderia, which have been found to degrade single- and multi-ring aromatic hydrocarbons [47], and Streptomyces and Nocardiodes that are considered the most representative genera of organic pesticide degrading bacteria [48]

Summary

C2 C3 S1 S2 S3 S4 S5 S6

Viruses with broad host ranges (viral contigs associated with multiple host taxa) were only detected in OCP-contaminated soils: 14 out of the total 26 viral contigs observed in OCP-contaminated soils were associated with a total of 23 bacterial taxa, mainly including Nocardioidaceae and Rhizobium. No potentially new virus-host links were found based on comparison with previously reported literature [20] or NCBI Genbank and JGI Viral Sequence databases Together these results suggest that viruses were associated with a higher number of bacterial hosts in OCPcontaminated compared to clean soils. Virus-encoded auxiliary genes are involved in both metabolism and pesticide degradation To explore the contribution of viruses for the ecology of bacterial communities, we compared the functional annotations of both bacterial and viral sequences in clean and OCP-contaminated soils. To investigate this in more detail, we compared bacteria- and virus-encoded carbohydrate-

Zheng et al 5

DISCUSSION

Findings

METHODS