Unveiling the gut microbiota and resistome of the wild cotton-mice, Peromyscus gossypinus, from heavy metal and radionuclide-contaminated sites in the Southeastern US

Authors: THOMAS, JESSE - Centers For Disease Control And Prevention (CDC) - United States; KIERAN, TROY - University Of Georgia; FINGER, JOHN - Auburn University; BAYONA-VASQUEZ, NATALIA - University Of Georgia; Oladeinde, Adelumola - Ade; BEASLEY, JAMES - University Of Georgia; SEAMAN, JOHN - University Of Georgia; MCARTHUR, J VAUN - University Of Georgia; RHODES, OLIN - University Of Georgia; GLENN, TRAVIS - University Of Georgia

Submitted to: American Society for Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/22/2021
Publication Date: 8/25/2021
Citation: Thomas, J.C., Kieran, T.J., Finger, J.W., Bayona-Vasquez, N.J., Oladeinde, A.A., Beasley, J., Seaman, J.C., Mcarthur, J., Rhodes, O.E., Glenn, T.C. 2021. Unveiling the gut microbiota and resistome of the wild cotton-mice, Peromyscus gossypinus, from heavy metal and radionuclide-contaminated sites in the Southeastern US. American Society for Microbiology. 9:e00097-21. https://doi.org/10.1128/Spectrum.00097-21.
DOI: https://doi.org/10.1128/Spectrum.00097-21

Interpretive Summary: To stop the increase in antibiotic resistant bacteria, it is important we understand if and how environmental contaminants such as metals contribute to the spread of antibiotic resistance genes. Bacterial exposure to metals has been demonstrated to be a predisposing factor for antibiotic resistance acquisition but how metals co-select for antibiotic resistance bacterial population is not fully understood. In this study, we compared the microbiome of mice captured from pristine sites to areas affected by legacies of heavy metals and radionuclide at the Savannah River Site. We identified an assortment of co-occurring antimicrobial and metal resistance genes in mice from all areas including sites without a history of contamination, but their abundance was higher in sites with radionuclide contamination. These results support previous studies and enhance our understanding of how metals can co-select for antibiotic resistance.

Technical Abstract: Antimicrobial resistance is a serious global public health concern because of its prevalence and ubiquitous distribution. The rapid dissemination of antibiotic resistant genes (ARGs) is thought to be the result of the massive overuse of antibiotics in agriculture and therapeutics. However, as previous studies have indicated, these are not the only sources of ARGs. There is a large body of evidence that has demonstrated that the dissemination of ARGs can also be influenced by heavy metal (HM) contamination. This co-selection phenomenon, whereby different resistance determinants are genetically linked on the same genetic element (co-resistance) or a single genetic element provides tolerance to multiple antimicrobial agents (cross-resistance) has profound clinical and environmental implications. In contrast to antibiotics, metals are not subject to degradation, and thus can persist in the environment as a selection pressure for long periods of time. While significant progress has been made to further characterize the influence of HMs on the enrichment and dissemination of ARGs in the environment, there is still much we do not know. To fill this knowledge gap, we present a comprehensive analysis of gut bacteria associated with wild cotton mouse, Peromyscus gossypinus, trapped from several areas affected by legacies of HM and radionuclide contamination. We explore how these contaminants affect gut microbial community (GMC) composition and diversity, and the enrichment of antibiotic, biocide, and metal-resistance genes. Although, we were able to identify that a myriad of co-occurring antimicrobial and HM resistance genes appear in mice from all areas including those without a history of contamination. The proportions of co-occurrence of ARGs and metal resistance genes (MRGs) is higher in sites with radionuclide contamination. These results support several previous studies and enhance our understanding of the co-selection process, while providing new insights into the ubiquity of antimicrobial resistance in the resistome of wild animals.