Unveiling the Gut Microbiota and Resistome of Wild Cotton Mice, Peromyscus gossypinus, from Heavy Metal- and Radionuclide-Contaminated Sites in the Southeastern United States
ABSTRACT The prevalence of antibiotic resistance genes (ARGs) can be driven by direct selection from antibiotic use and indirect selection from substances such as heavy metals (HMs). While significant progress has been made to characterize the influence of HMs on the enrichment and dissemination of...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2021-09-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/Spectrum.00097-21 |
| _version_ | 1818755127898537984 |
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| author | Jesse C. Thomas Troy J. Kieran John W. Finger Natalia J. Bayona-Vásquez Adelumola Oladeinde James C. Beasley John C. Seaman J. Vaun McArthur Olin E. Rhodes Travis C. Glenn |
| author_facet | Jesse C. Thomas Troy J. Kieran John W. Finger Natalia J. Bayona-Vásquez Adelumola Oladeinde James C. Beasley John C. Seaman J. Vaun McArthur Olin E. Rhodes Travis C. Glenn |
| author_sort | Jesse C. Thomas |
| collection | DOAJ |
| description | ABSTRACT The prevalence of antibiotic resistance genes (ARGs) can be driven by direct selection from antibiotic use and indirect selection from substances such as heavy metals (HMs). While significant progress has been made to 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 mice (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-occurring ARGs and metal resistance genes (MRGs) are higher in sites with radionuclide contamination. These results support those from several previous studies and enhance our understanding of the coselection process, while providing new insights into the ubiquity of antimicrobial resistance in the resistome of wild animals. IMPORTANCE Antimicrobial resistance is a serious global public health concern because of its prevalence and ubiquitous distribution. The rapid dissemination of antibiotic resistance genes is thought to be the result of the massive overuse of antibiotics in agriculture and therapeutics. However, previous studies have demonstrated that the spread of antibiotic resistance genes can also be influenced by heavy metal contamination. This coselection phenomenon, whereby different resistance determinants are genetically linked on the same genetic element (coresistance) or a single genetic element provides resistance to multiple antimicrobial agents (cross-resistance), has profound clinical and environmental implications. In contrast to antibiotics, heavy metals can persist in the environment as a selection pressure for long periods of time. Thus, it is important to understand how antibiotic resistance genes are distributed in the environment and to what extent heavy metal contaminants may be driving their selection, which we have done in one environmental setting. |
| first_indexed | 2024-12-18T05:34:13Z |
| format | Article |
| id | doaj.art-1db1205434824197a0bade31ba39130f |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-12-18T05:34:13Z |
| publishDate | 2021-09-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-1db1205434824197a0bade31ba39130f2022-12-21T21:19:21ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972021-09-019110.1128/Spectrum.00097-21Unveiling the Gut Microbiota and Resistome of Wild Cotton Mice, Peromyscus gossypinus, from Heavy Metal- and Radionuclide-Contaminated Sites in the Southeastern United StatesJesse C. Thomas0Troy J. Kieran1John W. Finger2Natalia J. Bayona-Vásquez3Adelumola Oladeinde4James C. Beasley5John C. Seaman6J. Vaun McArthur7Olin E. Rhodes8Travis C. Glenn9Department of Environmental Health Science, University of Georgia, Athens, Georgia, USADepartment of Environmental Health Science, University of Georgia, Athens, Georgia, USADepartment of Environmental Health Science, University of Georgia, Athens, Georgia, USADepartment of Environmental Health Science, University of Georgia, Athens, Georgia, USADepartment of Environmental Health Science, University of Georgia, Athens, Georgia, USASavannah River Ecology Laboratory, University of Georgia, Aiken, South Carolina, USASavannah River Ecology Laboratory, University of Georgia, Aiken, South Carolina, USASavannah River Ecology Laboratory, University of Georgia, Aiken, South Carolina, USASavannah River Ecology Laboratory, University of Georgia, Aiken, South Carolina, USADepartment of Environmental Health Science, University of Georgia, Athens, Georgia, USAABSTRACT The prevalence of antibiotic resistance genes (ARGs) can be driven by direct selection from antibiotic use and indirect selection from substances such as heavy metals (HMs). While significant progress has been made to 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 mice (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-occurring ARGs and metal resistance genes (MRGs) are higher in sites with radionuclide contamination. These results support those from several previous studies and enhance our understanding of the coselection process, while providing new insights into the ubiquity of antimicrobial resistance in the resistome of wild animals. IMPORTANCE Antimicrobial resistance is a serious global public health concern because of its prevalence and ubiquitous distribution. The rapid dissemination of antibiotic resistance genes is thought to be the result of the massive overuse of antibiotics in agriculture and therapeutics. However, previous studies have demonstrated that the spread of antibiotic resistance genes can also be influenced by heavy metal contamination. This coselection phenomenon, whereby different resistance determinants are genetically linked on the same genetic element (coresistance) or a single genetic element provides resistance to multiple antimicrobial agents (cross-resistance), has profound clinical and environmental implications. In contrast to antibiotics, heavy metals can persist in the environment as a selection pressure for long periods of time. Thus, it is important to understand how antibiotic resistance genes are distributed in the environment and to what extent heavy metal contaminants may be driving their selection, which we have done in one environmental setting.https://journals.asm.org/doi/10.1128/Spectrum.00097-21community structuregut microbiotaheavy metalsmetal resistanceantibiotic resistancecoselection |
| spellingShingle | Jesse C. Thomas Troy J. Kieran John W. Finger Natalia J. Bayona-Vásquez Adelumola Oladeinde James C. Beasley John C. Seaman J. Vaun McArthur Olin E. Rhodes Travis C. Glenn Unveiling the Gut Microbiota and Resistome of Wild Cotton Mice, Peromyscus gossypinus, from Heavy Metal- and Radionuclide-Contaminated Sites in the Southeastern United States Microbiology Spectrum community structure gut microbiota heavy metals metal resistance antibiotic resistance coselection |
| title | Unveiling the Gut Microbiota and Resistome of Wild Cotton Mice, Peromyscus gossypinus, from Heavy Metal- and Radionuclide-Contaminated Sites in the Southeastern United States |
| title_full | Unveiling the Gut Microbiota and Resistome of Wild Cotton Mice, Peromyscus gossypinus, from Heavy Metal- and Radionuclide-Contaminated Sites in the Southeastern United States |
| title_fullStr | Unveiling the Gut Microbiota and Resistome of Wild Cotton Mice, Peromyscus gossypinus, from Heavy Metal- and Radionuclide-Contaminated Sites in the Southeastern United States |
| title_full_unstemmed | Unveiling the Gut Microbiota and Resistome of Wild Cotton Mice, Peromyscus gossypinus, from Heavy Metal- and Radionuclide-Contaminated Sites in the Southeastern United States |
| title_short | Unveiling the Gut Microbiota and Resistome of Wild Cotton Mice, Peromyscus gossypinus, from Heavy Metal- and Radionuclide-Contaminated Sites in the Southeastern United States |
| title_sort | unveiling the gut microbiota and resistome of wild cotton mice peromyscus gossypinus from heavy metal and radionuclide contaminated sites in the southeastern united states |
| topic | community structure gut microbiota heavy metals metal resistance antibiotic resistance coselection |
| url | https://journals.asm.org/doi/10.1128/Spectrum.00097-21 |
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