Importance of anthropogenic sources at shaping the antimicrobial resistance profile of a peri-urban mesocarnivore

Katherine E.L. Worsley-Tonks; Elizabeth A. Miller; Chris L. Anchor; Jeff B. Bender; Stanley D. Gehrt; Shane C. McKenzie; Randall S. Singer; Timothy J. Johnson; Meggan E. Craft

doi:10.1016/j.scitotenv.2020.144166

Importance of anthropogenic sources at shaping the antimicrobial resistance profile of a peri-urban mesocarnivore

Katherine E.L. Worsley-Tonks, Elizabeth A. Miller, Chris L. Anchor, Jeff B. Bender, Stanley D. Gehrt, Shane C. McKenzie, Randall S. Singer, Timothy J. Johnson, Meggan E. Craft

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Abstract

Anthropogenically derived antimicrobial-resistant bacteria (ARB) and antimicrobial resistance genes (ARG) have been detected in wildlife. The likelihood of detecting ARB and ARG in wildlife increases with wildlife exposure to anthropogenic sources of antimicrobial resistance (AMR). Whether anthropogenic sources also increase the risk for AMR to spread in bacteria of wildlife is not well understood. The spread of AMR in bacteria of wildlife can be estimated by examining the richness of ARB and ARG, and the prevalence of ARB that have mobilizable ARG (i.e., ARG that can be transferred across bacteria via plasmids). Here, we investigated whether raccoons (Procyon lotor), with different exposures to anthropogenic sources, differed in prevalence and richness of extended-spectrum cephalosporin-resistant (ESC-R) Escherichia coli, richness of ARG present in ESC-R E. coli, and prevalence of ESC-R E. coli with plasmid-associated ARG. Sampling took place over the course of 10 months at seven sites in Chicago, USA. ESC-R E. coli were isolated from over half of the 211 raccoons sampled and were more likely to be isolated from urban than suburban raccoons. When examining the whole-genome sequences of ESC-R E. coli, 56 sequence types were identified, most of which were associated with the ARG bla_CMY and bla_CTX-M. A greater richness of ESC-R E. coli sequence types was found at sites with a wastewater treatment plant (WWTP) than without, but no difference was detected based on urban context. ARG richness in ESC-R E. coli did not significantly vary by urban context nor with presence of a WWTP. Importantly, ESC-R E. coli carrying plasmid-associated bla_CTX-M and bla_CMY ARG were more likely to be isolated from raccoons sampled at sites with a WWTP than without. Our findings indicate that anthropogenic sources may shape the AMR profile of wildlife, reinforcing the need to prevent dissemination of AMR into the environment.

Original language	English (US)
Article number	144166
Journal	Science of the Total Environment
Volume	764
DOIs	https://doi.org/10.1016/j.scitotenv.2020.144166
State	Published - Apr 10 2021

Bibliographical note

Funding Information:
Funding was provided by Donna Alexander from the Cook County Animal and Rabies Control , the Max McGraw Wildlife Foundation , the Forest Preserve District of Cook County , the National Science Foundation ( DEB-1413925 and 1654609 ), and CVM Research Office UMN Ag Experiment Station General Ag Research Funds ( MIN-62-098 ). The authors extend many thanks to the Gehrt lab for field and technical assistance, particularly Gretchen Anchor, Andy Burmesch, Yasmine Hentati, Lauren Ross, Katie Robertson, Missy Stallard, Sean Sullivan, Steven Winter, and Ashley Wurth. The authors also thank members of the Johnson lab, particularly Bonnie Weber, Alison Millis, and Emily Clarke for laboratory assistance. Finally, many thanks to the Minnesota Supercomputing Institute for bioinformatic support.

Publisher Copyright:
© 2020 Elsevier B.V.

Keywords

Antimicrobial resistance genes
Cephalosporin
Plasmid
Urbanization
Wastewater treatment plant
Wildlife

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UN SDGs

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Worsley-Tonks, K. E. L., Miller, E. A., Anchor, C. L., Bender, J. B., Gehrt, S. D., McKenzie, S. C., Singer, R. S., Johnson, T. J., & Craft, M. E. (2021). Importance of anthropogenic sources at shaping the antimicrobial resistance profile of a peri-urban mesocarnivore. Science of the Total Environment, 764, Article 144166. https://doi.org/10.1016/j.scitotenv.2020.144166

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abstract = "Anthropogenically derived antimicrobial-resistant bacteria (ARB) and antimicrobial resistance genes (ARG) have been detected in wildlife. The likelihood of detecting ARB and ARG in wildlife increases with wildlife exposure to anthropogenic sources of antimicrobial resistance (AMR). Whether anthropogenic sources also increase the risk for AMR to spread in bacteria of wildlife is not well understood. The spread of AMR in bacteria of wildlife can be estimated by examining the richness of ARB and ARG, and the prevalence of ARB that have mobilizable ARG (i.e., ARG that can be transferred across bacteria via plasmids). Here, we investigated whether raccoons (Procyon lotor), with different exposures to anthropogenic sources, differed in prevalence and richness of extended-spectrum cephalosporin-resistant (ESC-R) Escherichia coli, richness of ARG present in ESC-R E. coli, and prevalence of ESC-R E. coli with plasmid-associated ARG. Sampling took place over the course of 10 months at seven sites in Chicago, USA. ESC-R E. coli were isolated from over half of the 211 raccoons sampled and were more likely to be isolated from urban than suburban raccoons. When examining the whole-genome sequences of ESC-R E. coli, 56 sequence types were identified, most of which were associated with the ARG blaCMY and blaCTX-M. A greater richness of ESC-R E. coli sequence types was found at sites with a wastewater treatment plant (WWTP) than without, but no difference was detected based on urban context. ARG richness in ESC-R E. coli did not significantly vary by urban context nor with presence of a WWTP. Importantly, ESC-R E. coli carrying plasmid-associated blaCTX-M and blaCMY ARG were more likely to be isolated from raccoons sampled at sites with a WWTP than without. Our findings indicate that anthropogenic sources may shape the AMR profile of wildlife, reinforcing the need to prevent dissemination of AMR into the environment.",

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author = "Worsley-Tonks, {Katherine E.L.} and Miller, {Elizabeth A.} and Anchor, {Chris L.} and Bender, {Jeff B.} and Gehrt, {Stanley D.} and McKenzie, {Shane C.} and Singer, {Randall S.} and Johnson, {Timothy J.} and Craft, {Meggan E.}",

note = "Funding Information: Funding was provided by Donna Alexander from the Cook County Animal and Rabies Control , the Max McGraw Wildlife Foundation , the Forest Preserve District of Cook County , the National Science Foundation ( DEB-1413925 and 1654609 ), and CVM Research Office UMN Ag Experiment Station General Ag Research Funds ( MIN-62-098 ). The authors extend many thanks to the Gehrt lab for field and technical assistance, particularly Gretchen Anchor, Andy Burmesch, Yasmine Hentati, Lauren Ross, Katie Robertson, Missy Stallard, Sean Sullivan, Steven Winter, and Ashley Wurth. The authors also thank members of the Johnson lab, particularly Bonnie Weber, Alison Millis, and Emily Clarke for laboratory assistance. Finally, many thanks to the Minnesota Supercomputing Institute for bioinformatic support. Publisher Copyright: {\textcopyright} 2020 Elsevier B.V.",

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AU - Gehrt, Stanley D.

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AU - Singer, Randall S.

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AU - Craft, Meggan E.

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N2 - Anthropogenically derived antimicrobial-resistant bacteria (ARB) and antimicrobial resistance genes (ARG) have been detected in wildlife. The likelihood of detecting ARB and ARG in wildlife increases with wildlife exposure to anthropogenic sources of antimicrobial resistance (AMR). Whether anthropogenic sources also increase the risk for AMR to spread in bacteria of wildlife is not well understood. The spread of AMR in bacteria of wildlife can be estimated by examining the richness of ARB and ARG, and the prevalence of ARB that have mobilizable ARG (i.e., ARG that can be transferred across bacteria via plasmids). Here, we investigated whether raccoons (Procyon lotor), with different exposures to anthropogenic sources, differed in prevalence and richness of extended-spectrum cephalosporin-resistant (ESC-R) Escherichia coli, richness of ARG present in ESC-R E. coli, and prevalence of ESC-R E. coli with plasmid-associated ARG. Sampling took place over the course of 10 months at seven sites in Chicago, USA. ESC-R E. coli were isolated from over half of the 211 raccoons sampled and were more likely to be isolated from urban than suburban raccoons. When examining the whole-genome sequences of ESC-R E. coli, 56 sequence types were identified, most of which were associated with the ARG blaCMY and blaCTX-M. A greater richness of ESC-R E. coli sequence types was found at sites with a wastewater treatment plant (WWTP) than without, but no difference was detected based on urban context. ARG richness in ESC-R E. coli did not significantly vary by urban context nor with presence of a WWTP. Importantly, ESC-R E. coli carrying plasmid-associated blaCTX-M and blaCMY ARG were more likely to be isolated from raccoons sampled at sites with a WWTP than without. Our findings indicate that anthropogenic sources may shape the AMR profile of wildlife, reinforcing the need to prevent dissemination of AMR into the environment.

AB - Anthropogenically derived antimicrobial-resistant bacteria (ARB) and antimicrobial resistance genes (ARG) have been detected in wildlife. The likelihood of detecting ARB and ARG in wildlife increases with wildlife exposure to anthropogenic sources of antimicrobial resistance (AMR). Whether anthropogenic sources also increase the risk for AMR to spread in bacteria of wildlife is not well understood. The spread of AMR in bacteria of wildlife can be estimated by examining the richness of ARB and ARG, and the prevalence of ARB that have mobilizable ARG (i.e., ARG that can be transferred across bacteria via plasmids). Here, we investigated whether raccoons (Procyon lotor), with different exposures to anthropogenic sources, differed in prevalence and richness of extended-spectrum cephalosporin-resistant (ESC-R) Escherichia coli, richness of ARG present in ESC-R E. coli, and prevalence of ESC-R E. coli with plasmid-associated ARG. Sampling took place over the course of 10 months at seven sites in Chicago, USA. ESC-R E. coli were isolated from over half of the 211 raccoons sampled and were more likely to be isolated from urban than suburban raccoons. When examining the whole-genome sequences of ESC-R E. coli, 56 sequence types were identified, most of which were associated with the ARG blaCMY and blaCTX-M. A greater richness of ESC-R E. coli sequence types was found at sites with a wastewater treatment plant (WWTP) than without, but no difference was detected based on urban context. ARG richness in ESC-R E. coli did not significantly vary by urban context nor with presence of a WWTP. Importantly, ESC-R E. coli carrying plasmid-associated blaCTX-M and blaCMY ARG were more likely to be isolated from raccoons sampled at sites with a WWTP than without. Our findings indicate that anthropogenic sources may shape the AMR profile of wildlife, reinforcing the need to prevent dissemination of AMR into the environment.

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KW - Cephalosporin

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KW - Urbanization

KW - Wastewater treatment plant

KW - Wildlife

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Importance of anthropogenic sources at shaping the antimicrobial resistance profile of a peri-urban mesocarnivore

Abstract

Bibliographical note

Keywords

PubMed: MeSH publication types

UN SDGs

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