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Complex interactions between diverse mobile genetic elements drive the evolution of metal-resistant bacterial genomes |
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| Authors: | Khandaker Rayhan Mahbub Caroline Chénard Steven Batinovic Steve Petrovski Federico M Lauro Md Hafizur Rahman Mallavarapu Megharaj Ashley E Franks Maurizio Labbate |
| Institution: | 1. School of Life Sciences, University of Technology Sydney, Ultimo, New South Wales, Australia;2. Asian School for the Environment, Nanyang Technological University, Singapore, Singapore
Contribution: Writing - review & editing, Visualization, Formal analysis, Methodology;3. Division of Materials Science and Chemical Engineering, Yokohama National University, Yokohama, Kanagawa, Japan Contribution: Formal analysis, Writing - review & editing;4. Department of Physiology, Anatomy and Microbiology, La Trobe University, Bundoora, Victoria, Australia;5. Asian School for the Environment, Nanyang Technological University, Singapore, Singapore;6. School of Life Sciences, University of Technology Sydney, Ultimo, New South Wales, Australia Contribution: Visualization, Writing - review & editing;7. Global Centre for Environmental Remediation, College of Engineering, Science and Environment, The University of Newcastle, Callaghan, Australia Cooperative Research Centre for Contamination Assessment and Remediation of Environment, The University of Newcastle (UoN), Callaghan, New South Wales, Australia Contribution: Writing - review & editing, Resources |
| 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. |
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