Evolutionary dynamics of multidrug resistant Salmonella enterica serovar 4,[5],12:i:- in Australia

Danielle J Ingle; Rebecca L Ambrose; Sarah L Baines; Sebastian Duchene; Anders Gonçalves da Silva; Darren Y J Lee; Miriam Jones; Mary Valcanis; George Taiaroa; Susan A Ballard; Martyn D Kirk; Benjamin P Howden; Jaclyn S Pearson; Deborah A Williamson

doi:10.1038/s41467-021-25073-w

Evolutionary dynamics of multidrug resistant Salmonella enterica serovar 4,[5],12:i:- in Australia

Danielle J Ingle^*, Rebecca L Ambrose, Sarah L Baines, Sebastian Duchene, Anders Gonçalves da Silva, Darren Y J Lee, Miriam Jones, Mary Valcanis, George Taiaroa, Susan A Ballard, Martyn D Kirk, Benjamin P Howden, Jaclyn S Pearson, Deborah A Williamson^*

^*Corresponding author for this work

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

Abstract

Salmonella enterica serovar 4,[5],12:i:- (Salmonella 4,[5],12:i:-) is a monophasic variant of Salmonella Typhimurium that has emerged as a global cause of multidrug resistant salmonellosis. We used Bayesian phylodynamics, genomic epidemiology, and phenotypic characterization to describe the emergence and evolution of Salmonella 4,[5],12:i:- in Australia. We show that the interruption of the genetic region surrounding the phase II flagellin, FljB, causing a monophasic phenotype, represents a stepwise evolutionary event through the accumulation of mobile resistance elements with minimal impairment to bacterial fitness. We identify three lineages with different population dynamics and discrete antimicrobial resistance profiles emerged, likely reflecting differential antimicrobial selection pressures. Two lineages are associated with travel to South-East Asia and the third lineage is endemic to Australia. Moreover antimicrobial-resistant Salmonella 4,[5],12:i- lineages efficiently infected and survived in host phagocytes and epithelial cells without eliciting significant cellular cytotoxicity, suggesting a suppression of host immune response that may facilitate the persistence of Salmonella 4,[5],12:i:-.

Original language	English
Pages (from-to)	4786
Journal	Nature Communications
Volume	12
Issue number	1
DOIs	https://doi.org/10.1038/s41467-021-25073-w
Publication status	Published - 9 Aug 2021

Keywords

Anti-Bacterial Agents/pharmacology
Australia
Bayes Theorem
Cell Line
Drug Resistance, Multiple, Bacterial/drug effects
Evolution, Molecular
Flagellin/genetics
Humans
Immunity
Metals, Heavy/pharmacology
Phylogeny
Salmonella enterica/classification
Salmonella typhimurium
Serogroup
THP-1 Cells
Whole Genome Sequencing

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Ingle, D. J., Ambrose, R. L., Baines, S. L., Duchene, S., Gonçalves da Silva, A., Lee, D. Y. J., Jones, M., Valcanis, M., Taiaroa, G., Ballard, S. A., Kirk, M. D., Howden, B. P., Pearson, J. S., & Williamson, D. A. (2021). Evolutionary dynamics of multidrug resistant Salmonella enterica serovar 4,[5],12:i:- in Australia. Nature Communications, 12(1), 4786. https://doi.org/10.1038/s41467-021-25073-w

@article{b96bf987558b41b8966c3d8eff80a097,

title = "Evolutionary dynamics of multidrug resistant Salmonella enterica serovar 4,[5],12:i:- in Australia",

abstract = "Salmonella enterica serovar 4,[5],12:i:- (Salmonella 4,[5],12:i:-) is a monophasic variant of Salmonella Typhimurium that has emerged as a global cause of multidrug resistant salmonellosis. We used Bayesian phylodynamics, genomic epidemiology, and phenotypic characterization to describe the emergence and evolution of Salmonella 4,[5],12:i:- in Australia. We show that the interruption of the genetic region surrounding the phase II flagellin, FljB, causing a monophasic phenotype, represents a stepwise evolutionary event through the accumulation of mobile resistance elements with minimal impairment to bacterial fitness. We identify three lineages with different population dynamics and discrete antimicrobial resistance profiles emerged, likely reflecting differential antimicrobial selection pressures. Two lineages are associated with travel to South-East Asia and the third lineage is endemic to Australia. Moreover antimicrobial-resistant Salmonella 4,[5],12:i- lineages efficiently infected and survived in host phagocytes and epithelial cells without eliciting significant cellular cytotoxicity, suggesting a suppression of host immune response that may facilitate the persistence of Salmonella 4,[5],12:i:-.",

keywords = "Anti-Bacterial Agents/pharmacology, Australia, Bayes Theorem, Cell Line, Drug Resistance, Multiple, Bacterial/drug effects, Evolution, Molecular, Flagellin/genetics, Humans, Immunity, Metals, Heavy/pharmacology, Phylogeny, Salmonella enterica/classification, Salmonella typhimurium, Serogroup, THP-1 Cells, Whole Genome Sequencing",

author = "Ingle, {Danielle J} and Ambrose, {Rebecca L} and Baines, {Sarah L} and Sebastian Duchene and {Gon{\c c}alves da Silva}, Anders and Lee, {Darren Y J} and Miriam Jones and Mary Valcanis and George Taiaroa and Ballard, {Susan A} and Kirk, {Martyn D} and Howden, {Benjamin P} and Pearson, {Jaclyn S} and Williamson, {Deborah A}",

note = "This work was supported by the National Health and Medical Research Council (NHMRC), Australia Project Grant (APP1129770). D.J.I. is supported by an NHMRC Investigator Grant (APP1195210). S.D. was funded by the ARC (DE190100805). M.D.K. is supported by an NHMRC Career Development Fellowship (APP1145997). B.P.H. is supported by an NHMRC Investigator Grant (APP1196103). J.S.P. is supported by an NHMRC Career Development Fellowship (APP1159230). D.A.W. is supported by an NHMRC Investigator Grant (APP1174555). The Microbiological Diagnostic Unit Public Health Laboratory is funded by the Department of Health and Human Services, Victoria.",

year = "2021",

month = aug,

day = "9",

doi = "10.1038/s41467-021-25073-w",

language = "English",

volume = "12",

pages = "4786",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature publishing group",

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Ingle, DJ, Ambrose, RL, Baines, SL, Duchene, S, Gonçalves da Silva, A, Lee, DYJ, Jones, M, Valcanis, M, Taiaroa, G, Ballard, SA, Kirk, MD, Howden, BP, Pearson, JS & Williamson, DA 2021, 'Evolutionary dynamics of multidrug resistant Salmonella enterica serovar 4,[5],12:i:- in Australia', Nature Communications, vol. 12, no. 1, pp. 4786. https://doi.org/10.1038/s41467-021-25073-w

TY - JOUR

T1 - Evolutionary dynamics of multidrug resistant Salmonella enterica serovar 4,[5],12:i:- in Australia

AU - Ingle, Danielle J

AU - Ambrose, Rebecca L

AU - Baines, Sarah L

AU - Duchene, Sebastian

AU - Gonçalves da Silva, Anders

AU - Lee, Darren Y J

AU - Jones, Miriam

AU - Valcanis, Mary

AU - Taiaroa, George

AU - Ballard, Susan A

AU - Kirk, Martyn D

AU - Howden, Benjamin P

AU - Pearson, Jaclyn S

AU - Williamson, Deborah A

N1 - This work was supported by the National Health and Medical Research Council (NHMRC), Australia Project Grant (APP1129770). D.J.I. is supported by an NHMRC Investigator Grant (APP1195210). S.D. was funded by the ARC (DE190100805). M.D.K. is supported by an NHMRC Career Development Fellowship (APP1145997). B.P.H. is supported by an NHMRC Investigator Grant (APP1196103). J.S.P. is supported by an NHMRC Career Development Fellowship (APP1159230). D.A.W. is supported by an NHMRC Investigator Grant (APP1174555). The Microbiological Diagnostic Unit Public Health Laboratory is funded by the Department of Health and Human Services, Victoria.

PY - 2021/8/9

Y1 - 2021/8/9

N2 - Salmonella enterica serovar 4,[5],12:i:- (Salmonella 4,[5],12:i:-) is a monophasic variant of Salmonella Typhimurium that has emerged as a global cause of multidrug resistant salmonellosis. We used Bayesian phylodynamics, genomic epidemiology, and phenotypic characterization to describe the emergence and evolution of Salmonella 4,[5],12:i:- in Australia. We show that the interruption of the genetic region surrounding the phase II flagellin, FljB, causing a monophasic phenotype, represents a stepwise evolutionary event through the accumulation of mobile resistance elements with minimal impairment to bacterial fitness. We identify three lineages with different population dynamics and discrete antimicrobial resistance profiles emerged, likely reflecting differential antimicrobial selection pressures. Two lineages are associated with travel to South-East Asia and the third lineage is endemic to Australia. Moreover antimicrobial-resistant Salmonella 4,[5],12:i- lineages efficiently infected and survived in host phagocytes and epithelial cells without eliciting significant cellular cytotoxicity, suggesting a suppression of host immune response that may facilitate the persistence of Salmonella 4,[5],12:i:-.

AB - Salmonella enterica serovar 4,[5],12:i:- (Salmonella 4,[5],12:i:-) is a monophasic variant of Salmonella Typhimurium that has emerged as a global cause of multidrug resistant salmonellosis. We used Bayesian phylodynamics, genomic epidemiology, and phenotypic characterization to describe the emergence and evolution of Salmonella 4,[5],12:i:- in Australia. We show that the interruption of the genetic region surrounding the phase II flagellin, FljB, causing a monophasic phenotype, represents a stepwise evolutionary event through the accumulation of mobile resistance elements with minimal impairment to bacterial fitness. We identify three lineages with different population dynamics and discrete antimicrobial resistance profiles emerged, likely reflecting differential antimicrobial selection pressures. Two lineages are associated with travel to South-East Asia and the third lineage is endemic to Australia. Moreover antimicrobial-resistant Salmonella 4,[5],12:i- lineages efficiently infected and survived in host phagocytes and epithelial cells without eliciting significant cellular cytotoxicity, suggesting a suppression of host immune response that may facilitate the persistence of Salmonella 4,[5],12:i:-.

KW - Anti-Bacterial Agents/pharmacology

KW - Australia

KW - Bayes Theorem

KW - Cell Line

KW - Drug Resistance, Multiple, Bacterial/drug effects

KW - Evolution, Molecular

KW - Flagellin/genetics

KW - Humans

KW - Immunity

KW - Metals, Heavy/pharmacology

KW - Phylogeny

KW - Salmonella enterica/classification

KW - Salmonella typhimurium

KW - Serogroup

KW - THP-1 Cells

KW - Whole Genome Sequencing

U2 - 10.1038/s41467-021-25073-w

DO - 10.1038/s41467-021-25073-w

M3 - Article

C2 - 34373455

SN - 2041-1723

VL - 12

SP - 4786

JO - Nature Communications

JF - Nature Communications

IS - 1

ER -

Evolutionary dynamics of multidrug resistant Salmonella enterica serovar 4,[5],12:i:- in Australia

Abstract

Keywords

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