Gene exchange drives the ecological success of a multi-host bacterial pathogen

Emily J. Richardson, Rodrigo Bacigalupe, Ewan M. Harrison, Lucy A. Weinert, Samantha Lycett, Manouk Vrieling, Kirsty Robb, Paul A. Hoskisson, Matthew TG Holden, Edward J. Feil, Gavin K. Patterson, Steven YC Tong, Adebayo Shittu, Willen van Wamel, David M. Aanensen, Julian Parkhill, Sharon J. Peacock, Jukka Corander, Mark Holmes, J. Ross Fitzgerald

Research output: Contribution to journalArticle

Abstract

The capacity for some pathogens to jump into different host-species populations is a major threat to public health and food security. Staphylococcus aureus is a multi-host bacterial pathogen responsible for important human and livestock diseases. Here, using a population genomic approach we identify humans as a major hub for ancient and recent S. aureus host-switch events linked to the emergence of endemic livestock strains, and cows as the main animal reservoir for the emergence of human epidemic clones. Such host-species transitions are associated with horizontal acquisition of genetic elements from host-specific gene pools conferring traits required for survival in the new host-niche. Importantly, genes associated with antimicrobial resistance are unevenly distributed among human and animal hosts reflecting distinct antibiotic usage practices in medicine and agriculture. In addition to gene acquisition, genetic diversification has occurred in pathways associated with nutrient acquisition, implying metabolic remodeling after a host-switch in response to distinct nutrient availability. For example, S. aureus from dairy cattle exhibit enhanced utilization of lactose, a major source of carbohydrate in bovine milk. Overall, our findings highlight the influence of human activities on the multi-host ecology of a major bacterial pathogen, underpinned by horizontal gene transfer and core genome diversification.
LanguageEnglish
Pages1-43
Number of pages43
JournalNature Ecology & Evolution
Publication statusAccepted/In press - 25 Jun 2018

Fingerprint

pathogen
gene
pathogens
genes
Staphylococcus aureus
livestock
livestock diseases
animal
gene transfer
food security
nutrient availability
human diseases
antibiotic resistance
antibiotics
medicine
milk
lactose
dairy cattle
public health
cattle

Keywords

  • evolution
  • Staphylococcus aureus
  • host-species
  • adaptation
  • genomics

Cite this

Richardson, E. J., Bacigalupe, R., Harrison, E. M., Weinert, L. A., Lycett, S., Vrieling, M., ... Fitzgerald, J. R. (Accepted/In press). Gene exchange drives the ecological success of a multi-host bacterial pathogen. Nature Ecology & Evolution, 1-43.
Richardson, Emily J. ; Bacigalupe, Rodrigo ; Harrison, Ewan M. ; Weinert, Lucy A. ; Lycett, Samantha ; Vrieling, Manouk ; Robb, Kirsty ; Hoskisson, Paul A. ; Holden, Matthew TG ; Feil, Edward J. ; Patterson, Gavin K. ; Tong, Steven YC ; Shittu, Adebayo ; van Wamel, Willen ; Aanensen, David M. ; Parkhill, Julian ; Peacock, Sharon J. ; Corander, Jukka ; Holmes, Mark ; Fitzgerald, J. Ross. / Gene exchange drives the ecological success of a multi-host bacterial pathogen. In: Nature Ecology & Evolution. 2018 ; pp. 1-43.
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Richardson, EJ, Bacigalupe, R, Harrison, EM, Weinert, LA, Lycett, S, Vrieling, M, Robb, K, Hoskisson, PA, Holden, MTG, Feil, EJ, Patterson, GK, Tong, SYC, Shittu, A, van Wamel, W, Aanensen, DM, Parkhill, J, Peacock, SJ, Corander, J, Holmes, M & Fitzgerald, JR 2018, 'Gene exchange drives the ecological success of a multi-host bacterial pathogen' Nature Ecology & Evolution, pp. 1-43.

Gene exchange drives the ecological success of a multi-host bacterial pathogen. / Richardson, Emily J.; Bacigalupe, Rodrigo; Harrison, Ewan M.; Weinert, Lucy A.; Lycett, Samantha; Vrieling, Manouk; Robb, Kirsty; Hoskisson, Paul A.; Holden, Matthew TG; Feil, Edward J.; Patterson, Gavin K.; Tong, Steven YC; Shittu, Adebayo; van Wamel, Willen; Aanensen, David M.; Parkhill, Julian; Peacock, Sharon J.; Corander, Jukka; Holmes, Mark; Fitzgerald, J. Ross.

In: Nature Ecology & Evolution, 25.06.2018, p. 1-43.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Gene exchange drives the ecological success of a multi-host bacterial pathogen

AU - Richardson, Emily J.

AU - Bacigalupe, Rodrigo

AU - Harrison, Ewan M.

AU - Weinert, Lucy A.

AU - Lycett, Samantha

AU - Vrieling, Manouk

AU - Robb, Kirsty

AU - Hoskisson, Paul A.

AU - Holden, Matthew TG

AU - Feil, Edward J.

AU - Patterson, Gavin K.

AU - Tong, Steven YC

AU - Shittu, Adebayo

AU - van Wamel, Willen

AU - Aanensen, David M.

AU - Parkhill, Julian

AU - Peacock, Sharon J.

AU - Corander, Jukka

AU - Holmes, Mark

AU - Fitzgerald, J. Ross

PY - 2018/6/25

Y1 - 2018/6/25

N2 - The capacity for some pathogens to jump into different host-species populations is a major threat to public health and food security. Staphylococcus aureus is a multi-host bacterial pathogen responsible for important human and livestock diseases. Here, using a population genomic approach we identify humans as a major hub for ancient and recent S. aureus host-switch events linked to the emergence of endemic livestock strains, and cows as the main animal reservoir for the emergence of human epidemic clones. Such host-species transitions are associated with horizontal acquisition of genetic elements from host-specific gene pools conferring traits required for survival in the new host-niche. Importantly, genes associated with antimicrobial resistance are unevenly distributed among human and animal hosts reflecting distinct antibiotic usage practices in medicine and agriculture. In addition to gene acquisition, genetic diversification has occurred in pathways associated with nutrient acquisition, implying metabolic remodeling after a host-switch in response to distinct nutrient availability. For example, S. aureus from dairy cattle exhibit enhanced utilization of lactose, a major source of carbohydrate in bovine milk. Overall, our findings highlight the influence of human activities on the multi-host ecology of a major bacterial pathogen, underpinned by horizontal gene transfer and core genome diversification.

AB - The capacity for some pathogens to jump into different host-species populations is a major threat to public health and food security. Staphylococcus aureus is a multi-host bacterial pathogen responsible for important human and livestock diseases. Here, using a population genomic approach we identify humans as a major hub for ancient and recent S. aureus host-switch events linked to the emergence of endemic livestock strains, and cows as the main animal reservoir for the emergence of human epidemic clones. Such host-species transitions are associated with horizontal acquisition of genetic elements from host-specific gene pools conferring traits required for survival in the new host-niche. Importantly, genes associated with antimicrobial resistance are unevenly distributed among human and animal hosts reflecting distinct antibiotic usage practices in medicine and agriculture. In addition to gene acquisition, genetic diversification has occurred in pathways associated with nutrient acquisition, implying metabolic remodeling after a host-switch in response to distinct nutrient availability. For example, S. aureus from dairy cattle exhibit enhanced utilization of lactose, a major source of carbohydrate in bovine milk. Overall, our findings highlight the influence of human activities on the multi-host ecology of a major bacterial pathogen, underpinned by horizontal gene transfer and core genome diversification.

KW - evolution

KW - Staphylococcus aureus

KW - host-species

KW - adaptation

KW - genomics

UR - https://www.nature.com/natecolevol/

M3 - Article

SP - 1

EP - 43

JO - Nature Ecology & Evolution

T2 - Nature Ecology & Evolution

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ER -

Richardson EJ, Bacigalupe R, Harrison EM, Weinert LA, Lycett S, Vrieling M et al. Gene exchange drives the ecological success of a multi-host bacterial pathogen. Nature Ecology & Evolution. 2018 Jun 25;1-43.