Whole-genome epidemiology links phage-mediated acquisition of a virulence gene to the clonal expansion of a pandemic salmonella enterica serovar typhimurium clone

Eleonora Tassinari; Matt Bawn; Gaetan Thilliez; Oliver Charity; Luke Acton; Mark Kirkwood; Liljana Petrovska; Timothy Dallman; Catherine M. Burgess; Neil Hall; Geraldine Duffy; Robert A. Kingsley

doi:10.1099/mgen.0.000456

Whole-genome epidemiology links phage-mediated acquisition of a virulence gene to the clonal expansion of a pandemic salmonella enterica serovar typhimurium clone

Eleonora Tassinari, Matt Bawn, Gaetan Thilliez, Oliver Charity, Luke Acton, Mark Kirkwood, Liljana Petrovska, Timothy Dallman, Catherine M. Burgess, Neil Hall, Geraldine Duffy, Robert A. Kingsley^*

^*Corresponding author for this work

Gastrointestinal Bacteria WGS

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

20 Citations (Scopus)

17 Downloads (Pure)

Abstract

Epidemic and pandemic clones of bacterial pathogens with distinct characteristics continually emerge, replacing those previously dominant through mechanisms that remain poorly characterized. Here, whole-genome-sequencing-powered epidemiology linked horizontal transfer of a virulence gene, sopE, to the emergence and clonal expansion of a new epidemic Salmonella enterica serovar Typhimurium (S. Typhimurium) clone. The sopE gene is sporadically distributed within the genus Salmonella and rare in S. enterica Typhimurium lineages, but was acquired multiple times during clonal expansion of the currently dominant pandemic monophasic S. Typhimurium sequence type (ST) 34 clone. Ancestral state reconstruction and time-scaled phylogenetic analysis indicated that sopE was not present in the common ancestor of the epidemic clade, but later acquisition resulted in increased clonal expansion of sopE-containing clones that was temporally associated with emergence of the epidemic, consistent with increased fitness. The sopE gene was mainly associated with a temperate bacteriophage mTmV, but recombination with other bacteriophage and apparent horizontal gene transfer of the sopE gene cassette resulted in distribution among at least four mobile genetic elements within the monophasic S. enterica Typhimurium ST34 epidemic clade. The mTmV prophage lysogenic transfer to other S. enterica serovars in vitro was limited, but included the common pig-associated S. enterica Derby (S. Derby). This may explain mTmV in S. Derby co-circulating on farms with monophasic S. Typhimurium ST34, highlighting the potential for further transfer of the sopE virulence gene in nature. We conclude that whole-genome epidemiology pinpoints potential drivers of evolutionary and epidemiological dynamics during pathogen emergence, and identifies targets for subsequent research in epidemiology and bacterial pathogenesis.

Original language	English
Article number	000456
Pages (from-to)	1-15
Number of pages	15
Journal	Microbial Genomics
Volume	6
Issue number	11
DOIs	https://doi.org/10.1099/mgen.0.000456
Publication status	Published - 28 Oct 2020

Bibliographical note

Funding Information: R.K. was supported by Biotechnology and Biological Sciences Research Council (BBSRC) research grants BB/N007964/1 and BB/M025489/1, and by the BBSRC Institute Strategic Programme ? Microbes in the Food Chain BB/R012504/1 and its constituent projects BBS/E/F/000PR10348 and BBS/E/F/000PR10349. The postgraduate studies of E.T. were funded by Teagasc Walsh Fellowship 2015028.

Open Access: This is an open-access article distributed under the terms of the Creative Commons Attribution License.

Publisher Copyright: © 2020 The Authors.

Citation: Tassinari, Eleonora, et al. "Whole-genome epidemiology links phage-mediated acquisition of a virulence gene to the clonal expansion of a pandemic Salmonella enterica serovar Typhimurium clone." Microbial genomics 6.11 (2020).

DOI: https://doi.org/10.1099/mgen.0.000456

Keywords

Epidemic
Evolution
Phylogenomics
Salmonella
SopE

Access to Document

10.1099/mgen.0.000456Licence: CC BY

Tassinari2020Whole-GenomeEpidemiologyLinksPhage-MediatedAcquisitionMicrobGenomFinal published version, 4.42 MBLicence: CC BY

Cite this

Tassinari, E., Bawn, M., Thilliez, G., Charity, O., Acton, L., Kirkwood, M., Petrovska, L., Dallman, T., Burgess, C. M., Hall, N., Duffy, G., & Kingsley, R. A. (2020). Whole-genome epidemiology links phage-mediated acquisition of a virulence gene to the clonal expansion of a pandemic salmonella enterica serovar typhimurium clone. Microbial Genomics, 6(11), 1-15. Article 000456. https://doi.org/10.1099/mgen.0.000456

@article{e2f8c226f2534a94b54c1551e0956f27,

title = "Whole-genome epidemiology links phage-mediated acquisition of a virulence gene to the clonal expansion of a pandemic salmonella enterica serovar typhimurium clone",

abstract = "Epidemic and pandemic clones of bacterial pathogens with distinct characteristics continually emerge, replacing those previously dominant through mechanisms that remain poorly characterized. Here, whole-genome-sequencing-powered epidemiology linked horizontal transfer of a virulence gene, sopE, to the emergence and clonal expansion of a new epidemic Salmonella enterica serovar Typhimurium (S. Typhimurium) clone. The sopE gene is sporadically distributed within the genus Salmonella and rare in S. enterica Typhimurium lineages, but was acquired multiple times during clonal expansion of the currently dominant pandemic monophasic S. Typhimurium sequence type (ST) 34 clone. Ancestral state reconstruction and time-scaled phylogenetic analysis indicated that sopE was not present in the common ancestor of the epidemic clade, but later acquisition resulted in increased clonal expansion of sopE-containing clones that was temporally associated with emergence of the epidemic, consistent with increased fitness. The sopE gene was mainly associated with a temperate bacteriophage mTmV, but recombination with other bacteriophage and apparent horizontal gene transfer of the sopE gene cassette resulted in distribution among at least four mobile genetic elements within the monophasic S. enterica Typhimurium ST34 epidemic clade. The mTmV prophage lysogenic transfer to other S. enterica serovars in vitro was limited, but included the common pig-associated S. enterica Derby (S. Derby). This may explain mTmV in S. Derby co-circulating on farms with monophasic S. Typhimurium ST34, highlighting the potential for further transfer of the sopE virulence gene in nature. We conclude that whole-genome epidemiology pinpoints potential drivers of evolutionary and epidemiological dynamics during pathogen emergence, and identifies targets for subsequent research in epidemiology and bacterial pathogenesis.",

keywords = "Epidemic, Evolution, Phylogenomics, Salmonella, SopE",

author = "Eleonora Tassinari and Matt Bawn and Gaetan Thilliez and Oliver Charity and Luke Acton and Mark Kirkwood and Liljana Petrovska and Timothy Dallman and Burgess, {Catherine M.} and Neil Hall and Geraldine Duffy and Kingsley, {Robert A.}",

note = "Funding Information: R.K. was supported by Biotechnology and Biological Sciences Research Council (BBSRC) research grants BB/N007964/1 and BB/M025489/1, and by the BBSRC Institute Strategic Programme ? Microbes in the Food Chain BB/R012504/1 and its constituent projects BBS/E/F/000PR10348 and BBS/E/F/000PR10349. The postgraduate studies of E.T. were funded by Teagasc Walsh Fellowship 2015028. Open Access: This is an open-access article distributed under the terms of the Creative Commons Attribution License. Publisher Copyright: {\textcopyright} 2020 The Authors. Citation: Tassinari, Eleonora, et al. {"}Whole-genome epidemiology links phage-mediated acquisition of a virulence gene to the clonal expansion of a pandemic Salmonella enterica serovar Typhimurium clone.{"} Microbial genomics 6.11 (2020). DOI: https://doi.org/10.1099/mgen.0.000456 ",

year = "2020",

month = oct,

day = "28",

doi = "10.1099/mgen.0.000456",

language = "English",

volume = "6",

pages = "1--15",

journal = "Microbial Genomics",

issn = "2057-5858",

publisher = "Microbiology Society",

number = "11",

}

Tassinari, E, Bawn, M, Thilliez, G, Charity, O, Acton, L, Kirkwood, M, Petrovska, L, Dallman, T, Burgess, CM, Hall, N, Duffy, G & Kingsley, RA 2020, 'Whole-genome epidemiology links phage-mediated acquisition of a virulence gene to the clonal expansion of a pandemic salmonella enterica serovar typhimurium clone', Microbial Genomics, vol. 6, no. 11, 000456, pp. 1-15. https://doi.org/10.1099/mgen.0.000456

TY - JOUR

T1 - Whole-genome epidemiology links phage-mediated acquisition of a virulence gene to the clonal expansion of a pandemic salmonella enterica serovar typhimurium clone

AU - Tassinari, Eleonora

AU - Bawn, Matt

AU - Thilliez, Gaetan

AU - Charity, Oliver

AU - Acton, Luke

AU - Kirkwood, Mark

AU - Petrovska, Liljana

AU - Dallman, Timothy

AU - Burgess, Catherine M.

AU - Hall, Neil

AU - Duffy, Geraldine

AU - Kingsley, Robert A.

N1 - Funding Information: R.K. was supported by Biotechnology and Biological Sciences Research Council (BBSRC) research grants BB/N007964/1 and BB/M025489/1, and by the BBSRC Institute Strategic Programme ? Microbes in the Food Chain BB/R012504/1 and its constituent projects BBS/E/F/000PR10348 and BBS/E/F/000PR10349. The postgraduate studies of E.T. were funded by Teagasc Walsh Fellowship 2015028. Open Access: This is an open-access article distributed under the terms of the Creative Commons Attribution License. Publisher Copyright: © 2020 The Authors. Citation: Tassinari, Eleonora, et al. "Whole-genome epidemiology links phage-mediated acquisition of a virulence gene to the clonal expansion of a pandemic Salmonella enterica serovar Typhimurium clone." Microbial genomics 6.11 (2020). DOI: https://doi.org/10.1099/mgen.0.000456

PY - 2020/10/28

Y1 - 2020/10/28

N2 - Epidemic and pandemic clones of bacterial pathogens with distinct characteristics continually emerge, replacing those previously dominant through mechanisms that remain poorly characterized. Here, whole-genome-sequencing-powered epidemiology linked horizontal transfer of a virulence gene, sopE, to the emergence and clonal expansion of a new epidemic Salmonella enterica serovar Typhimurium (S. Typhimurium) clone. The sopE gene is sporadically distributed within the genus Salmonella and rare in S. enterica Typhimurium lineages, but was acquired multiple times during clonal expansion of the currently dominant pandemic monophasic S. Typhimurium sequence type (ST) 34 clone. Ancestral state reconstruction and time-scaled phylogenetic analysis indicated that sopE was not present in the common ancestor of the epidemic clade, but later acquisition resulted in increased clonal expansion of sopE-containing clones that was temporally associated with emergence of the epidemic, consistent with increased fitness. The sopE gene was mainly associated with a temperate bacteriophage mTmV, but recombination with other bacteriophage and apparent horizontal gene transfer of the sopE gene cassette resulted in distribution among at least four mobile genetic elements within the monophasic S. enterica Typhimurium ST34 epidemic clade. The mTmV prophage lysogenic transfer to other S. enterica serovars in vitro was limited, but included the common pig-associated S. enterica Derby (S. Derby). This may explain mTmV in S. Derby co-circulating on farms with monophasic S. Typhimurium ST34, highlighting the potential for further transfer of the sopE virulence gene in nature. We conclude that whole-genome epidemiology pinpoints potential drivers of evolutionary and epidemiological dynamics during pathogen emergence, and identifies targets for subsequent research in epidemiology and bacterial pathogenesis.

AB - Epidemic and pandemic clones of bacterial pathogens with distinct characteristics continually emerge, replacing those previously dominant through mechanisms that remain poorly characterized. Here, whole-genome-sequencing-powered epidemiology linked horizontal transfer of a virulence gene, sopE, to the emergence and clonal expansion of a new epidemic Salmonella enterica serovar Typhimurium (S. Typhimurium) clone. The sopE gene is sporadically distributed within the genus Salmonella and rare in S. enterica Typhimurium lineages, but was acquired multiple times during clonal expansion of the currently dominant pandemic monophasic S. Typhimurium sequence type (ST) 34 clone. Ancestral state reconstruction and time-scaled phylogenetic analysis indicated that sopE was not present in the common ancestor of the epidemic clade, but later acquisition resulted in increased clonal expansion of sopE-containing clones that was temporally associated with emergence of the epidemic, consistent with increased fitness. The sopE gene was mainly associated with a temperate bacteriophage mTmV, but recombination with other bacteriophage and apparent horizontal gene transfer of the sopE gene cassette resulted in distribution among at least four mobile genetic elements within the monophasic S. enterica Typhimurium ST34 epidemic clade. The mTmV prophage lysogenic transfer to other S. enterica serovars in vitro was limited, but included the common pig-associated S. enterica Derby (S. Derby). This may explain mTmV in S. Derby co-circulating on farms with monophasic S. Typhimurium ST34, highlighting the potential for further transfer of the sopE virulence gene in nature. We conclude that whole-genome epidemiology pinpoints potential drivers of evolutionary and epidemiological dynamics during pathogen emergence, and identifies targets for subsequent research in epidemiology and bacterial pathogenesis.

KW - Epidemic

KW - Evolution

KW - Phylogenomics

KW - Salmonella

KW - SopE

UR - http://www.scopus.com/inward/record.url?scp=85097003584&partnerID=8YFLogxK

U2 - 10.1099/mgen.0.000456

DO - 10.1099/mgen.0.000456

M3 - Article

C2 - 33112226

AN - SCOPUS:85097003584

SN - 2057-5858

VL - 6

SP - 1

EP - 15

JO - Microbial Genomics

JF - Microbial Genomics

IS - 11

M1 - 000456

ER -

Whole-genome epidemiology links phage-mediated acquisition of a virulence gene to the clonal expansion of a pandemic salmonella enterica serovar typhimurium clone

Abstract

Bibliographical note

Keywords

Access to Document

Other files and links

Fingerprint

Cite this