Long-term maintenance of multidrug-resistant Escherichia coli carried by vampire bats and shared with livestock in Peru

Julio A. Benavides; Sylvain Godreuil; Andrés Opazo-Capurro; Oumar O. Mahamat; Nestor Falcon; Katarina Oravcova; Daniel G. Streicker; Carlos Shiva

doi:10.1016/j.scitotenv.2021.152045

Long-term maintenance of multidrug-resistant Escherichia coli carried by vampire bats and shared with livestock in Peru

Julio A. Benavides
, Sylvain Godreuil
, Andrés Opazo-Capurro
, Oumar O. Mahamat
, Nestor Falcon
, Katarina Oravcova
, Daniel G. Streicker
, Carlos Shiva

Facultad de Ciencias de la Vida
University of Glasgow
MICROB-R
Centre Hospitalier Universitaire de Montpellier
Université de Montpellier
Institut de Recherche Pour le Développement, UMR177 IRD/CIR AD INTERTRYP
Universidad de Concepción
Service de laboratoire Hôpital de la Mère et de l'Enfant
Univ. Nacional Mayor de San Marcos
MRC-University of Glasgow Centre for Virus Research

Research output: Contribution to journal › Article › peer-review

43 Scopus citations

Abstract

Extended-spectrum beta-lactamase-producing Escherichia coli (ESBL-E. coli) have been reported in wildlife worldwide. Whether wildlife is a transient host of ESBL-E. coli or comprises an independently maintained reservoir is unknown. We investigated this question by longitudinally monitoring ESBL-E. coli in common vampire bats and nearby livestock in Peru. Among 388 bats from five vampire bat colonies collected over three years, ESBL-E. coli were detected at a low prevalence (10% in 2015, 4% in 2017 and 2018) compared to a high prevalence (48%) from 134 livestock sampled in 2017. All ESBL-E. coli were multidrug-resistant, and whole genome sequencing of 33 randomly selected ESBL-E. coli isolates (18 recovered from bats) detected 46 genes conferring resistance to antibiotics including third-generation cephalosporins (e.g., bla_CTX-M-55, bla_CTX-M-15, bla_CTX-M-65, bla_CTX-M-3, bla_CTX-M-14), aminoglycosides, fluoroquinolones, and colistin (mcr-1). The mcr-1 gene is reported for the first time on a wild bat in Latin America. ESBL-E. coli also carried 31 plasmid replicon types and 16 virulence genes. Twenty-three E. coli sequence types (STs) were detected, including STs involved in clinical infections worldwide (e.g., ST 167, ST 117, ST 10, ST 156 and ST 648). ESBL-E. coli with identical cgMLST (ST 167) were detected in the same bat roost in 2015 and 2017, and several ESBL-E. coli from different bat roosts clustered together in the cgMLST reconstruction, suggesting long-term maintenance of ESBL-E. coli within bats. Most antibiotic resistance and virulence genes were detected in E. coli from both host populations, while ESBL-E. coli ST 744 was found in a bat and a pig from the same locality, suggesting possible cross-species exchanges of genetic material and/or bacteria between bats and livestock. This study suggests that wild mammals can maintain multidrug-resistant bacteria and share them with livestock.

Original language	English
Article number	152045
Journal	Science of the Total Environment
Volume	810
DOIs	https://doi.org/10.1016/j.scitotenv.2021.152045
State	Published - 1 Mar 2022
Externally published	Yes

Keywords

Antimicrobial resistance
E. coli
Extended-spectrum beta-lactamase
Latin America
Wildlife
mcr-1

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10.1016/j.scitotenv.2021.152045

Cite this

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title = "Long-term maintenance of multidrug-resistant Escherichia coli carried by vampire bats and shared with livestock in Peru",

abstract = "Extended-spectrum beta-lactamase-producing Escherichia coli (ESBL-E. coli) have been reported in wildlife worldwide. Whether wildlife is a transient host of ESBL-E. coli or comprises an independently maintained reservoir is unknown. We investigated this question by longitudinally monitoring ESBL-E. coli in common vampire bats and nearby livestock in Peru. Among 388 bats from five vampire bat colonies collected over three years, ESBL-E. coli were detected at a low prevalence (10\% in 2015, 4\% in 2017 and 2018) compared to a high prevalence (48\%) from 134 livestock sampled in 2017. All ESBL-E. coli were multidrug-resistant, and whole genome sequencing of 33 randomly selected ESBL-E. coli isolates (18 recovered from bats) detected 46 genes conferring resistance to antibiotics including third-generation cephalosporins (e.g., blaCTX-M-55, blaCTX-M-15, blaCTX-M-65, blaCTX-M-3, blaCTX-M-14), aminoglycosides, fluoroquinolones, and colistin (mcr-1). The mcr-1 gene is reported for the first time on a wild bat in Latin America. ESBL-E. coli also carried 31 plasmid replicon types and 16 virulence genes. Twenty-three E. coli sequence types (STs) were detected, including STs involved in clinical infections worldwide (e.g., ST 167, ST 117, ST 10, ST 156 and ST 648). ESBL-E. coli with identical cgMLST (ST 167) were detected in the same bat roost in 2015 and 2017, and several ESBL-E. coli from different bat roosts clustered together in the cgMLST reconstruction, suggesting long-term maintenance of ESBL-E. coli within bats. Most antibiotic resistance and virulence genes were detected in E. coli from both host populations, while ESBL-E. coli ST 744 was found in a bat and a pig from the same locality, suggesting possible cross-species exchanges of genetic material and/or bacteria between bats and livestock. This study suggests that wild mammals can maintain multidrug-resistant bacteria and share them with livestock.",

keywords = "Antimicrobial resistance, E. coli, Extended-spectrum beta-lactamase, Latin America, Wildlife, mcr-1",

author = "Benavides, \{Julio A.\} and Sylvain Godreuil and Andr{\'e}s Opazo-Capurro and Mahamat, \{Oumar O.\} and Nestor Falcon and Katarina Oravcova and Streicker, \{Daniel G.\} and Carlos Shiva",

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doi = "10.1016/j.scitotenv.2021.152045",

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T1 - Long-term maintenance of multidrug-resistant Escherichia coli carried by vampire bats and shared with livestock in Peru

AU - Benavides, Julio A.

AU - Godreuil, Sylvain

AU - Opazo-Capurro, Andrés

AU - Mahamat, Oumar O.

AU - Falcon, Nestor

AU - Oravcova, Katarina

AU - Streicker, Daniel G.

AU - Shiva, Carlos

PY - 2022/3/1

Y1 - 2022/3/1

N2 - Extended-spectrum beta-lactamase-producing Escherichia coli (ESBL-E. coli) have been reported in wildlife worldwide. Whether wildlife is a transient host of ESBL-E. coli or comprises an independently maintained reservoir is unknown. We investigated this question by longitudinally monitoring ESBL-E. coli in common vampire bats and nearby livestock in Peru. Among 388 bats from five vampire bat colonies collected over three years, ESBL-E. coli were detected at a low prevalence (10% in 2015, 4% in 2017 and 2018) compared to a high prevalence (48%) from 134 livestock sampled in 2017. All ESBL-E. coli were multidrug-resistant, and whole genome sequencing of 33 randomly selected ESBL-E. coli isolates (18 recovered from bats) detected 46 genes conferring resistance to antibiotics including third-generation cephalosporins (e.g., blaCTX-M-55, blaCTX-M-15, blaCTX-M-65, blaCTX-M-3, blaCTX-M-14), aminoglycosides, fluoroquinolones, and colistin (mcr-1). The mcr-1 gene is reported for the first time on a wild bat in Latin America. ESBL-E. coli also carried 31 plasmid replicon types and 16 virulence genes. Twenty-three E. coli sequence types (STs) were detected, including STs involved in clinical infections worldwide (e.g., ST 167, ST 117, ST 10, ST 156 and ST 648). ESBL-E. coli with identical cgMLST (ST 167) were detected in the same bat roost in 2015 and 2017, and several ESBL-E. coli from different bat roosts clustered together in the cgMLST reconstruction, suggesting long-term maintenance of ESBL-E. coli within bats. Most antibiotic resistance and virulence genes were detected in E. coli from both host populations, while ESBL-E. coli ST 744 was found in a bat and a pig from the same locality, suggesting possible cross-species exchanges of genetic material and/or bacteria between bats and livestock. This study suggests that wild mammals can maintain multidrug-resistant bacteria and share them with livestock.

AB - Extended-spectrum beta-lactamase-producing Escherichia coli (ESBL-E. coli) have been reported in wildlife worldwide. Whether wildlife is a transient host of ESBL-E. coli or comprises an independently maintained reservoir is unknown. We investigated this question by longitudinally monitoring ESBL-E. coli in common vampire bats and nearby livestock in Peru. Among 388 bats from five vampire bat colonies collected over three years, ESBL-E. coli were detected at a low prevalence (10% in 2015, 4% in 2017 and 2018) compared to a high prevalence (48%) from 134 livestock sampled in 2017. All ESBL-E. coli were multidrug-resistant, and whole genome sequencing of 33 randomly selected ESBL-E. coli isolates (18 recovered from bats) detected 46 genes conferring resistance to antibiotics including third-generation cephalosporins (e.g., blaCTX-M-55, blaCTX-M-15, blaCTX-M-65, blaCTX-M-3, blaCTX-M-14), aminoglycosides, fluoroquinolones, and colistin (mcr-1). The mcr-1 gene is reported for the first time on a wild bat in Latin America. ESBL-E. coli also carried 31 plasmid replicon types and 16 virulence genes. Twenty-three E. coli sequence types (STs) were detected, including STs involved in clinical infections worldwide (e.g., ST 167, ST 117, ST 10, ST 156 and ST 648). ESBL-E. coli with identical cgMLST (ST 167) were detected in the same bat roost in 2015 and 2017, and several ESBL-E. coli from different bat roosts clustered together in the cgMLST reconstruction, suggesting long-term maintenance of ESBL-E. coli within bats. Most antibiotic resistance and virulence genes were detected in E. coli from both host populations, while ESBL-E. coli ST 744 was found in a bat and a pig from the same locality, suggesting possible cross-species exchanges of genetic material and/or bacteria between bats and livestock. This study suggests that wild mammals can maintain multidrug-resistant bacteria and share them with livestock.

KW - Antimicrobial resistance

KW - E. coli

KW - Extended-spectrum beta-lactamase

KW - Latin America

KW - Wildlife

KW - mcr-1

UR - https://www.scopus.com/pages/publications/85120936923

U2 - 10.1016/j.scitotenv.2021.152045

DO - 10.1016/j.scitotenv.2021.152045

M3 - Artículo

C2 - 34883172

AN - SCOPUS:85120936923

SN - 0048-9697

VL - 810

JO - Science of the Total Environment

JF - Science of the Total Environment

M1 - 152045

ER -

Long-term maintenance of multidrug-resistant Escherichia coli carried by vampire bats and shared with livestock in Peru

Abstract

Keywords

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