Gene pool transmission of multidrug resistance among Campylobacter from livestock, sewage and human disease

Evangelos Mourkas; Diego Florez-Cuadrado; Ben Pascoe; Jessica K. Calland; Sion C. Bayliss; Leonardos Mageiros; Guillaume Méric; Matthew D. Hitchings; Alberto Quesada; Concepción Porrero; María Ugarte-Ruiz; José Gutiérrez-Fernández; Lucas Domínguez; Samuel K. Sheppard

doi:10.1111/1462-2920.14760

Gene pool transmission of multidrug resistance among Campylobacter from livestock, sewage and human disease

Evangelos Mourkas, Diego Florez-Cuadrado, Ben Pascoe, Jessica K. Calland, Sion C. Bayliss, Leonardos Mageiros, Guillaume Méric, Matthew D. Hitchings, Alberto Quesada, Concepción Porrero, María Ugarte-Ruiz, José Gutiérrez-Fernández, Lucas Domínguez, Samuel K. Sheppard^*

^*Corresponding author for this work

Research output: Contribution to journal › Article (Academic Journal) › peer-review

60 Citations (Scopus)

Abstract

The use of antimicrobials in human and veterinary medicine has coincided with a rise in antimicrobial resistance (AMR) in the food-borne pathogens Campylobacter jejuni and Campylobacter coli. Faecal contamination from the main reservoir hosts (livestock, especially poultry) is the principal route of human infection but little is known about the spread of AMR among source and sink populations. In particular, questions remain about how Campylobacter resistomes interact between species and hosts, and the potential role of sewage as a conduit for the spread of AMR. Here, we investigate the genomic variation associated with AMR in 168 C. jejuni and 92 C. coli strains isolated from humans, livestock and urban effluents in Spain. AMR was tested in vitro and isolate genomes were sequenced and screened for putative AMR genes and alleles. Genes associated with resistance to multiple drug classes were observed in both species and were commonly present in multidrug-resistant genomic islands (GIs), often located on plasmids or mobile elements. In many cases, these loci had alleles that were shared among C. jejuni and C. coli consistent with horizontal transfer. Our results suggest that specific antibiotic resistance genes have spread among Campylobacter isolated from humans, animals and the environment.

Original language	English
Pages (from-to)	4597-4613
Number of pages	17
Journal	Environmental Microbiology
Volume	21
Issue number	12
DOIs	https://doi.org/10.1111/1462-2920.14760
Publication status	Published - 1 Dec 2019

Bibliographical note

Funding Information:
S.K.S., B.P. and S.C.B. were supported by grants from the Medical Research Council (MR/L015080/1), the Wellcome Trust (088786/C/09/Z), the Food Standards Agency (FS246004) and the Biotechnology and Biological Sciences Research Council (BB/I02464X/1). E.M. received a University of Bath Faculty of Science URSA studentship. D.F.C. is supported by the FPI program (BES-2013-065003) from the Spanish Ministry of Economy and Competitiveness. J.K.C. is supported by a BBSRC KTN PhD studentship (BB/P504750/1). All high performance computing was conducted with MRC CLIMB. We wish to thank our technicians Mar?a Garc?a, Estefan?a Rivero and Nisrin Maasoumi for their excellent technical assistance.

Publisher Copyright:
© 2019 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.1111/1462-2920.14760

Handle.net

Persistent link

Cite this

Mourkas, E., Florez-Cuadrado, D., Pascoe, B., Calland, J. K., Bayliss, S. C., Mageiros, L., Méric, G., Hitchings, M. D., Quesada, A., Porrero, C., Ugarte-Ruiz, M., Gutiérrez-Fernández, J., Domínguez, L., & Sheppard, S. K. (2019). Gene pool transmission of multidrug resistance among Campylobacter from livestock, sewage and human disease. Environmental Microbiology, 21(12), 4597-4613. https://doi.org/10.1111/1462-2920.14760

@article{956ed1c81d604647b705d9eece7b315e,

title = "Gene pool transmission of multidrug resistance among Campylobacter from livestock, sewage and human disease",

abstract = "The use of antimicrobials in human and veterinary medicine has coincided with a rise in antimicrobial resistance (AMR) in the food-borne pathogens Campylobacter jejuni and Campylobacter coli. Faecal contamination from the main reservoir hosts (livestock, especially poultry) is the principal route of human infection but little is known about the spread of AMR among source and sink populations. In particular, questions remain about how Campylobacter resistomes interact between species and hosts, and the potential role of sewage as a conduit for the spread of AMR. Here, we investigate the genomic variation associated with AMR in 168 C. jejuni and 92 C. coli strains isolated from humans, livestock and urban effluents in Spain. AMR was tested in vitro and isolate genomes were sequenced and screened for putative AMR genes and alleles. Genes associated with resistance to multiple drug classes were observed in both species and were commonly present in multidrug-resistant genomic islands (GIs), often located on plasmids or mobile elements. In many cases, these loci had alleles that were shared among C. jejuni and C. coli consistent with horizontal transfer. Our results suggest that specific antibiotic resistance genes have spread among Campylobacter isolated from humans, animals and the environment.",

author = "Evangelos Mourkas and Diego Florez-Cuadrado and Ben Pascoe and Calland, {Jessica K.} and Bayliss, {Sion C.} and Leonardos Mageiros and Guillaume M{\'e}ric and Hitchings, {Matthew D.} and Alberto Quesada and Concepci{\'o}n Porrero and Mar{\'i}a Ugarte-Ruiz and Jos{\'e} Guti{\'e}rrez-Fern{\'a}ndez and Lucas Dom{\'i}nguez and Sheppard, {Samuel K.}",

note = "Funding Information: S.K.S., B.P. and S.C.B. were supported by grants from the Medical Research Council (MR/L015080/1), the Wellcome Trust (088786/C/09/Z), the Food Standards Agency (FS246004) and the Biotechnology and Biological Sciences Research Council (BB/I02464X/1). E.M. received a University of Bath Faculty of Science URSA studentship. D.F.C. is supported by the FPI program (BES-2013-065003) from the Spanish Ministry of Economy and Competitiveness. J.K.C. is supported by a BBSRC KTN PhD studentship (BB/P504750/1). All high performance computing was conducted with MRC CLIMB. We wish to thank our technicians Mar?a Garc?a, Estefan?a Rivero and Nisrin Maasoumi for their excellent technical assistance. Publisher Copyright: {\textcopyright} 2019 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.",

year = "2019",

month = dec,

day = "1",

doi = "10.1111/1462-2920.14760",

language = "English",

volume = "21",

pages = "4597--4613",

journal = "Environmental Microbiology",

issn = "1462-2912",

publisher = "Wiley",

number = "12",

}

Mourkas, E, Florez-Cuadrado, D, Pascoe, B, Calland, JK, Bayliss, SC, Mageiros, L, Méric, G, Hitchings, MD, Quesada, A, Porrero, C, Ugarte-Ruiz, M, Gutiérrez-Fernández, J, Domínguez, L & Sheppard, SK 2019, 'Gene pool transmission of multidrug resistance among Campylobacter from livestock, sewage and human disease', Environmental Microbiology, vol. 21, no. 12, pp. 4597-4613. https://doi.org/10.1111/1462-2920.14760

TY - JOUR

T1 - Gene pool transmission of multidrug resistance among Campylobacter from livestock, sewage and human disease

AU - Mourkas, Evangelos

AU - Florez-Cuadrado, Diego

AU - Pascoe, Ben

AU - Calland, Jessica K.

AU - Bayliss, Sion C.

AU - Mageiros, Leonardos

AU - Méric, Guillaume

AU - Hitchings, Matthew D.

AU - Quesada, Alberto

AU - Porrero, Concepción

AU - Ugarte-Ruiz, María

AU - Gutiérrez-Fernández, José

AU - Domínguez, Lucas

AU - Sheppard, Samuel K.

N1 - Funding Information: S.K.S., B.P. and S.C.B. were supported by grants from the Medical Research Council (MR/L015080/1), the Wellcome Trust (088786/C/09/Z), the Food Standards Agency (FS246004) and the Biotechnology and Biological Sciences Research Council (BB/I02464X/1). E.M. received a University of Bath Faculty of Science URSA studentship. D.F.C. is supported by the FPI program (BES-2013-065003) from the Spanish Ministry of Economy and Competitiveness. J.K.C. is supported by a BBSRC KTN PhD studentship (BB/P504750/1). All high performance computing was conducted with MRC CLIMB. We wish to thank our technicians Mar?a Garc?a, Estefan?a Rivero and Nisrin Maasoumi for their excellent technical assistance. Publisher Copyright: © 2019 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.

PY - 2019/12/1

Y1 - 2019/12/1

N2 - The use of antimicrobials in human and veterinary medicine has coincided with a rise in antimicrobial resistance (AMR) in the food-borne pathogens Campylobacter jejuni and Campylobacter coli. Faecal contamination from the main reservoir hosts (livestock, especially poultry) is the principal route of human infection but little is known about the spread of AMR among source and sink populations. In particular, questions remain about how Campylobacter resistomes interact between species and hosts, and the potential role of sewage as a conduit for the spread of AMR. Here, we investigate the genomic variation associated with AMR in 168 C. jejuni and 92 C. coli strains isolated from humans, livestock and urban effluents in Spain. AMR was tested in vitro and isolate genomes were sequenced and screened for putative AMR genes and alleles. Genes associated with resistance to multiple drug classes were observed in both species and were commonly present in multidrug-resistant genomic islands (GIs), often located on plasmids or mobile elements. In many cases, these loci had alleles that were shared among C. jejuni and C. coli consistent with horizontal transfer. Our results suggest that specific antibiotic resistance genes have spread among Campylobacter isolated from humans, animals and the environment.

AB - The use of antimicrobials in human and veterinary medicine has coincided with a rise in antimicrobial resistance (AMR) in the food-borne pathogens Campylobacter jejuni and Campylobacter coli. Faecal contamination from the main reservoir hosts (livestock, especially poultry) is the principal route of human infection but little is known about the spread of AMR among source and sink populations. In particular, questions remain about how Campylobacter resistomes interact between species and hosts, and the potential role of sewage as a conduit for the spread of AMR. Here, we investigate the genomic variation associated with AMR in 168 C. jejuni and 92 C. coli strains isolated from humans, livestock and urban effluents in Spain. AMR was tested in vitro and isolate genomes were sequenced and screened for putative AMR genes and alleles. Genes associated with resistance to multiple drug classes were observed in both species and were commonly present in multidrug-resistant genomic islands (GIs), often located on plasmids or mobile elements. In many cases, these loci had alleles that were shared among C. jejuni and C. coli consistent with horizontal transfer. Our results suggest that specific antibiotic resistance genes have spread among Campylobacter isolated from humans, animals and the environment.

UR - http://www.scopus.com/inward/record.url?scp=85071327340&partnerID=8YFLogxK

U2 - 10.1111/1462-2920.14760

DO - 10.1111/1462-2920.14760

M3 - Article (Academic Journal)

C2 - 31385413

AN - SCOPUS:85071327340

SN - 1462-2912

VL - 21

SP - 4597

EP - 4613

JO - Environmental Microbiology

JF - Environmental Microbiology

IS - 12

ER -

Gene pool transmission of multidrug resistance among Campylobacter from livestock, sewage and human disease

Abstract

Bibliographical note

UN SDGs

Access to Document

Handle.net

Other files and links

Fingerprint

Cite this