Genomic Characterization of Fecal <i>Escherichia coli</i> Isolates with Reduced Susceptibility to Beta-Lactam Antimicrobials from Wild Hogs and Coyotes

This study was carried out to determine the antimicrobial resistance (AMR) genes and mobile genetic elements of 16 <i>Escherichia coli</i> isolates—with reduced susceptibility to ceftazidime and imipenem—that were recovered from the fecal samples of coyotes and wild hogs from West Texas,...

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Main Authors: Babafela Awosile, Jason Fritzler, Gizem Levent, Md. Kaisar Rahman, Samuel Ajulo, Ian Daniel, Yamima Tasnim, Sumon Sarkar
Format: Article
Language:English
Published: MDPI AG 2023-07-01
Series:Pathogens
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Online Access:https://www.mdpi.com/2076-0817/12/7/929
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author Babafela Awosile
Jason Fritzler
Gizem Levent
Md. Kaisar Rahman
Samuel Ajulo
Ian Daniel
Yamima Tasnim
Sumon Sarkar
author_facet Babafela Awosile
Jason Fritzler
Gizem Levent
Md. Kaisar Rahman
Samuel Ajulo
Ian Daniel
Yamima Tasnim
Sumon Sarkar
author_sort Babafela Awosile
collection DOAJ
description This study was carried out to determine the antimicrobial resistance (AMR) genes and mobile genetic elements of 16 <i>Escherichia coli</i> isolates—with reduced susceptibility to ceftazidime and imipenem—that were recovered from the fecal samples of coyotes and wild hogs from West Texas, USA. Whole-genome sequencing data analyses revealed distinct isolates with a unique sequence type and serotype designation. Among 16 isolates, 4 isolates were multidrug resistant, and 5 isolates harbored at least 1 beta-lactamase gene (<i>bla</i><sub>CMY-2</sub>, <i>bla</i><sub>CTX-M-55</sub>, or <i>bla</i><sub>CTX-M-27</sub>) that confers resistance to beta-lactam antimicrobials. Several isolates carried genes conferring resistance to tetracyclines (<i>tet</i>(A), <i>tet</i>(B), and <i>tet</i>(C)), aminoglycosides (<i>aac(3)-IId</i>, <i>ant(3″)-Ia</i>, <i>aph(3′)-Ia</i>, <i>aph(3″)-lb</i>, <i>aadA5</i>, and <i>aph(6)-ld)</i>, sulfonamides (<i>sul1</i>, <i>sul2</i>, and <i>sul3</i>), amphenicol (<i>floR</i>), trimethoprim (<i>dfrA1</i> and <i>dfrA17</i>), and macrolide, lincosamide, and streptogramin B (MLSB) agents (<i>Inu(F)</i>, <i>erm(B)</i>, and <i>mph(A)</i>). Nine isolates showed chromosomal mutations in the promoter region G of ampC beta-lactamase gene, while three isolates showed mutations in <i>gyrA</i>, <i>parC</i>, and <i>parE</i> quinolone resistance-determining regions, which confer resistance to quinolones. We also detected seven incompatibility plasmid groups, with incF being the most common. Different types of virulence genes were detected, including those that enhance bacterial fitness and pathogenicity. One <i>bla</i><sub>CMY-2</sub> positive isolate (O8:H28) from a wild hog was also a Shiga toxin-producing <i>E. coli</i> and was a carrier of the stx2A virulence toxin subtype. We report the detection of <i>bla</i><sub>CMY-2</sub>, <i>bla</i><sub>CTX-M-55</sub>, and <i>bla</i><sub>CTX-M-27</sub> beta-lactamase genes in <i>E. coli</i> from coyotes for the first time. This study demonstrates the importance of wildlife as reservoirs of important multi-drug-resistant bacteria and provides information for future comparative genomic analysis with the limited literature on antimicrobial resistance dynamics in wildlife such as coyotes.
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spelling doaj.art-a6454359c29d41c2944551b1f30cb2002023-11-18T20:51:02ZengMDPI AGPathogens2076-08172023-07-0112792910.3390/pathogens12070929Genomic Characterization of Fecal <i>Escherichia coli</i> Isolates with Reduced Susceptibility to Beta-Lactam Antimicrobials from Wild Hogs and CoyotesBabafela Awosile0Jason Fritzler1Gizem Levent2Md. Kaisar Rahman3Samuel Ajulo4Ian Daniel5Yamima Tasnim6Sumon Sarkar7School of Veterinary Medicine, Texas Tech University, Amarillo, TX 79106, USASchool of Veterinary Medicine, Texas Tech University, Amarillo, TX 79106, USASchool of Veterinary Medicine, Texas Tech University, Amarillo, TX 79106, USASchool of Veterinary Medicine, Texas Tech University, Amarillo, TX 79106, USASchool of Veterinary Medicine, Texas Tech University, Amarillo, TX 79106, USASchool of Veterinary Medicine, Texas Tech University, Amarillo, TX 79106, USASchool of Veterinary Medicine, Texas Tech University, Amarillo, TX 79106, USASchool of Veterinary Medicine, Texas Tech University, Amarillo, TX 79106, USAThis study was carried out to determine the antimicrobial resistance (AMR) genes and mobile genetic elements of 16 <i>Escherichia coli</i> isolates—with reduced susceptibility to ceftazidime and imipenem—that were recovered from the fecal samples of coyotes and wild hogs from West Texas, USA. Whole-genome sequencing data analyses revealed distinct isolates with a unique sequence type and serotype designation. Among 16 isolates, 4 isolates were multidrug resistant, and 5 isolates harbored at least 1 beta-lactamase gene (<i>bla</i><sub>CMY-2</sub>, <i>bla</i><sub>CTX-M-55</sub>, or <i>bla</i><sub>CTX-M-27</sub>) that confers resistance to beta-lactam antimicrobials. Several isolates carried genes conferring resistance to tetracyclines (<i>tet</i>(A), <i>tet</i>(B), and <i>tet</i>(C)), aminoglycosides (<i>aac(3)-IId</i>, <i>ant(3″)-Ia</i>, <i>aph(3′)-Ia</i>, <i>aph(3″)-lb</i>, <i>aadA5</i>, and <i>aph(6)-ld)</i>, sulfonamides (<i>sul1</i>, <i>sul2</i>, and <i>sul3</i>), amphenicol (<i>floR</i>), trimethoprim (<i>dfrA1</i> and <i>dfrA17</i>), and macrolide, lincosamide, and streptogramin B (MLSB) agents (<i>Inu(F)</i>, <i>erm(B)</i>, and <i>mph(A)</i>). Nine isolates showed chromosomal mutations in the promoter region G of ampC beta-lactamase gene, while three isolates showed mutations in <i>gyrA</i>, <i>parC</i>, and <i>parE</i> quinolone resistance-determining regions, which confer resistance to quinolones. We also detected seven incompatibility plasmid groups, with incF being the most common. Different types of virulence genes were detected, including those that enhance bacterial fitness and pathogenicity. One <i>bla</i><sub>CMY-2</sub> positive isolate (O8:H28) from a wild hog was also a Shiga toxin-producing <i>E. coli</i> and was a carrier of the stx2A virulence toxin subtype. We report the detection of <i>bla</i><sub>CMY-2</sub>, <i>bla</i><sub>CTX-M-55</sub>, and <i>bla</i><sub>CTX-M-27</sub> beta-lactamase genes in <i>E. coli</i> from coyotes for the first time. This study demonstrates the importance of wildlife as reservoirs of important multi-drug-resistant bacteria and provides information for future comparative genomic analysis with the limited literature on antimicrobial resistance dynamics in wildlife such as coyotes.https://www.mdpi.com/2076-0817/12/7/929beta-lactam antimicrobial<i>E. coli</i>wild hogcoyote
spellingShingle Babafela Awosile
Jason Fritzler
Gizem Levent
Md. Kaisar Rahman
Samuel Ajulo
Ian Daniel
Yamima Tasnim
Sumon Sarkar
Genomic Characterization of Fecal <i>Escherichia coli</i> Isolates with Reduced Susceptibility to Beta-Lactam Antimicrobials from Wild Hogs and Coyotes
Pathogens
beta-lactam antimicrobial
<i>E. coli</i>
wild hog
coyote
title Genomic Characterization of Fecal <i>Escherichia coli</i> Isolates with Reduced Susceptibility to Beta-Lactam Antimicrobials from Wild Hogs and Coyotes
title_full Genomic Characterization of Fecal <i>Escherichia coli</i> Isolates with Reduced Susceptibility to Beta-Lactam Antimicrobials from Wild Hogs and Coyotes
title_fullStr Genomic Characterization of Fecal <i>Escherichia coli</i> Isolates with Reduced Susceptibility to Beta-Lactam Antimicrobials from Wild Hogs and Coyotes
title_full_unstemmed Genomic Characterization of Fecal <i>Escherichia coli</i> Isolates with Reduced Susceptibility to Beta-Lactam Antimicrobials from Wild Hogs and Coyotes
title_short Genomic Characterization of Fecal <i>Escherichia coli</i> Isolates with Reduced Susceptibility to Beta-Lactam Antimicrobials from Wild Hogs and Coyotes
title_sort genomic characterization of fecal i escherichia coli i isolates with reduced susceptibility to beta lactam antimicrobials from wild hogs and coyotes
topic beta-lactam antimicrobial
<i>E. coli</i>
wild hog
coyote
url https://www.mdpi.com/2076-0817/12/7/929
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