Complex interactions between diverse mobile genetic elements drive the evolution of metal‐resistant bacterial genomes

Abstract

In this study, we compared the genomes of three metal‐resistant bacteria isolated from mercury‐contaminated soil. We identified diverse and novel MGEs with evidence of multiple LGT events shaping their genomic structure and heavy metal resistance. Among the three metal‐resistant strains, Sphingobium sp SA2 and Sphingopyxis sp SE2 were resistant to multiple metals including mercury, cadmium, copper, zinc and lead. Pseudoxanthomonas sp SE1 showed resistance to mercury only. Whole genome sequencing by Illumina and Oxford Nanopore technologies was undertaken to obtain comprehensive genomic data. The Sphingobium and Sphingopyxis strains contained multiple chromosomes and plasmids, whereas the Pseudoxanthomonas strain contained one circular chromosome. Consistent with their metal resistance profiles, the strains of Sphingobium and Sphingopyxis contained a higher quantity of diverse metal resistance genes across their chromosomes and plasmids compared to the single‐metal resistant Pseudoxanthomonas SE1. In all three strains, metal resistance genes were principally associated with various novel MGEs including genomic islands (GIs), integrative conjugative elements (ICEs), transposons, insertion sequences (IS), recombinase in trio (RIT) elements and group II introns, indicating their importance in facilitating metal resistance adaptation in a contaminated environment. In the Pseudoxanthomonas strain, metal resistance regions were largely situated on a GI. The chromosomes of the strains of Sphingobium and Sphingopyxis contained multiple metal resistance regions, which were likely acquired by several GIs, ICEs, numerous IS elements, several Tn3 family transposons and RIT elements. Two of the plasmids of Sphingobium were impacted by Tn3 family transposons and ISs likely integrating metal resistance genes. The two plasmids of Sphingopyxis harboured transposons, IS elements, an RIT element and a group II intron. This study provides a comprehensive annotation of complex genomic regions of metal resistance associated with novel MGEs. It highlights the critical importance of LGT in the evolution of metal resistance of bacteria in contaminated environments.

Acquisition, Evolution, and Diversification of Genomic Islands: A Case Study of a Virulence Gene Cluster inPseudomonas syringae

“…Examples include multiresistance to antibiotics in P. aeruginosa , a major human pathogen (Moradali et al, 2017), resistance to heavy metals, and genes involved in plant pathogenicity. GInts share structural similarities and limited sequence identity with the Tn 554 -family, which are MGEs associated with multiresistance to antibiotics in Firmicutes (Ross et al, 2021); strand-biased circularizing integrative elements, involved in the spread of antimicrobial resistance among Gammaproteobacteria (Idola et al, 2023); and recombinase in trio elements, which are widespread in Bacteria and are involved in metal resistance (Ricker et al, 2013; Mahbub et al, 2023). Due to their sheer abundance (Audrey et al, 2023; Idola et al, 2023), all these elements constitute a vast and unexplored source of genetic variation in bacteria, whose activity can greatly impact human wellbeing.…”