Recombination-mediated host-adaptation by avian Staphylococcus aureus

Susan Murray; Ben Pascoe; Guillaume Méric; Leonardos Mageiros; Koji Yahara; Matthew D Hitchings; Yasmin Friedmann; Thomas S Wilkinson; Fraser J Gormley; Dietrich Mack; James E Bray; Sarah Lamble; Rory Bowden; Keith A Jolley; Martin C J Maiden; Sarah Wendlandt; Stefan Schwarz; Jukka Corander; Ross Fitzgerald; Samuel K Sheppard

doi:10.1093/gbe/evx037

Recombination-mediated host-adaptation by avian Staphylococcus aureus

Susan Murray, Ben Pascoe, Guillaume Méric, Leonardos Mageiros, Koji Yahara, Matthew D Hitchings, Yasmin Friedmann, Thomas S Wilkinson, Fraser J Gormley, Dietrich Mack, James E Bray, Sarah Lamble, Rory Bowden, Keith A Jolley, Martin C J Maiden, Sarah Wendlandt, Stefan Schwarz, Jukka Corander, Ross Fitzgerald, Samuel K Sheppard

Royal (Dick) School of Veterinary Studies

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

Abstract

Staphylococcus aureus are globally disseminated among farmed chickens causing skeletal muscle infections, dermatitis and septicaemia. The emergence of poultry-associated lineages has involved zoonotic transmission from humans to chickens but questions remain about the specific adaptations that promote proliferation of chicken pathogens. We characterised genetic variation in a population of genome-sequenced S. aureus isolates of poultry and human origin. Genealogical analysis identified a dominant poultry-associated sequence cluster within the CC5 clonal complex. Poultry and human CC5 isolates were significantly distinct from each other and more recombination events were detected in the poultry isolates. We identified forty-four recombination events in 33 genes along the branch extending to the poultry-specific CC5 cluster, and 47 genes were found more often in CC5 poultry isolates compared to those from humans. Many of these gene sequences were common in chicken isolates from other clonal complexes suggesting horizontal gene transfer among poultry associated lineages. Consistent with functional predictions for putative poultry-associated genes, poultry isolates showed enhanced growth at 42oC and greater erythrocyte lysis on chicken blood agar in comparison with human isolates. By combining phenotype information with evolutionary analysis of staphylococcal genomes, we provide evidence of adaptation, following a human-to-poultry host transition. This has important implications for the emergence and dissemination of new pathogenic clones associated with modern agriculture.

Original language	English
Pages (from-to)	830-842
Journal	Genome Biology and Evolution
Volume	9
Issue number	4
Early online date	28 Feb 2017
DOIs	https://doi.org/10.1093/gbe/evx037
Publication status	Published - 1 Apr 2017

Keywords / Materials (for Non-textual outputs)

Staphylococcus
Genomics
Poultry infection
Evolution
Recombination

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10.1093/gbe/evx037

Recombination-mediated host-adaptation by avian Staphylococcus aureus
This is an open access article distributed under the terms of the Creative Commons CC BY license, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Accepted author manuscript, 4.27 MBLicence: Creative Commons: Attribution (CC-BY)

Innate immunity and endemic diseases in livestock species
Collie, D. (Principal Investigator), Beard, P. (Co-investigator), Bishop, S. (Co-investigator), Bronsvoort, M. (Co-investigator), Burt, D. (Co-investigator), Fitzgerald, R. (Co-investigator), Freeman, T. (Co-investigator), Gally, D. (Co-investigator), Gill, A. (Co-investigator), Glass, E. (Co-investigator), Hocking, P. (Co-investigator), Hope, J. (Co-investigator), Hume, D. (Co-investigator), Kaiser, P. (Co-investigator), Mabbott, N. (Co-investigator), McLachlan, G. (Co-investigator), Morrison, L. (Co-investigator), Stevens, J. (Co-investigator), Stevens, M. (Co-investigator) & Watson, M. (Co-investigator)
BBSRC
1/04/12 → 31/03/17
Project: Research

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Murray, S., Pascoe, B., Méric, G., Mageiros, L., Yahara, K., Hitchings, M. D., Friedmann, Y., Wilkinson, T. S., Gormley, F. J., Mack, D., Bray, J. E., Lamble, S., Bowden, R., Jolley, K. A., Maiden, M. C. J., Wendlandt, S., Schwarz, S., Corander, J., Fitzgerald, R., & Sheppard, S. K. (2017). Recombination-mediated host-adaptation by avian Staphylococcus aureus. Genome Biology and Evolution, 9(4), 830-842. https://doi.org/10.1093/gbe/evx037

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title = "Recombination-mediated host-adaptation by avian Staphylococcus aureus",

abstract = "Staphylococcus aureus are globally disseminated among farmed chickens causing skeletal muscle infections, dermatitis and septicaemia. The emergence of poultry-associated lineages has involved zoonotic transmission from humans to chickens but questions remain about the specific adaptations that promote proliferation of chicken pathogens. We characterised genetic variation in a population of genome-sequenced S. aureus isolates of poultry and human origin. Genealogical analysis identified a dominant poultry-associated sequence cluster within the CC5 clonal complex. Poultry and human CC5 isolates were significantly distinct from each other and more recombination events were detected in the poultry isolates. We identified forty-four recombination events in 33 genes along the branch extending to the poultry-specific CC5 cluster, and 47 genes were found more often in CC5 poultry isolates compared to those from humans. Many of these gene sequences were common in chicken isolates from other clonal complexes suggesting horizontal gene transfer among poultry associated lineages. Consistent with functional predictions for putative poultry-associated genes, poultry isolates showed enhanced growth at 42oC and greater erythrocyte lysis on chicken blood agar in comparison with human isolates. By combining phenotype information with evolutionary analysis of staphylococcal genomes, we provide evidence of adaptation, following a human-to-poultry host transition. This has important implications for the emergence and dissemination of new pathogenic clones associated with modern agriculture.",

keywords = "Staphylococcus, Genomics, Poultry infection, Evolution, Recombination",

author = "Susan Murray and Ben Pascoe and Guillaume M{\'e}ric and Leonardos Mageiros and Koji Yahara and Hitchings, {Matthew D} and Yasmin Friedmann and Wilkinson, {Thomas S} and Gormley, {Fraser J} and Dietrich Mack and Bray, {James E} and Sarah Lamble and Rory Bowden and Jolley, {Keith A} and Maiden, {Martin C J} and Sarah Wendlandt and Stefan Schwarz and Jukka Corander and Ross Fitzgerald and Sheppard, {Samuel K}",

note = "{\textcopyright} The Author(s) 2017. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.",

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Murray, S, Pascoe, B, Méric, G, Mageiros, L, Yahara, K, Hitchings, MD, Friedmann, Y, Wilkinson, TS, Gormley, FJ, Mack, D, Bray, JE, Lamble, S, Bowden, R, Jolley, KA, Maiden, MCJ, Wendlandt, S, Schwarz, S, Corander, J, Fitzgerald, R & Sheppard, SK 2017, 'Recombination-mediated host-adaptation by avian Staphylococcus aureus', Genome Biology and Evolution, vol. 9, no. 4, pp. 830-842. https://doi.org/10.1093/gbe/evx037

TY - JOUR

T1 - Recombination-mediated host-adaptation by avian Staphylococcus aureus

AU - Murray, Susan

AU - Pascoe, Ben

AU - Méric, Guillaume

AU - Mageiros, Leonardos

AU - Yahara, Koji

AU - Hitchings, Matthew D

AU - Friedmann, Yasmin

AU - Wilkinson, Thomas S

AU - Gormley, Fraser J

AU - Mack, Dietrich

AU - Bray, James E

AU - Lamble, Sarah

AU - Bowden, Rory

AU - Jolley, Keith A

AU - Maiden, Martin C J

AU - Wendlandt, Sarah

AU - Schwarz, Stefan

AU - Corander, Jukka

AU - Fitzgerald, Ross

AU - Sheppard, Samuel K

N1 - © The Author(s) 2017. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

PY - 2017/4/1

Y1 - 2017/4/1

N2 - Staphylococcus aureus are globally disseminated among farmed chickens causing skeletal muscle infections, dermatitis and septicaemia. The emergence of poultry-associated lineages has involved zoonotic transmission from humans to chickens but questions remain about the specific adaptations that promote proliferation of chicken pathogens. We characterised genetic variation in a population of genome-sequenced S. aureus isolates of poultry and human origin. Genealogical analysis identified a dominant poultry-associated sequence cluster within the CC5 clonal complex. Poultry and human CC5 isolates were significantly distinct from each other and more recombination events were detected in the poultry isolates. We identified forty-four recombination events in 33 genes along the branch extending to the poultry-specific CC5 cluster, and 47 genes were found more often in CC5 poultry isolates compared to those from humans. Many of these gene sequences were common in chicken isolates from other clonal complexes suggesting horizontal gene transfer among poultry associated lineages. Consistent with functional predictions for putative poultry-associated genes, poultry isolates showed enhanced growth at 42oC and greater erythrocyte lysis on chicken blood agar in comparison with human isolates. By combining phenotype information with evolutionary analysis of staphylococcal genomes, we provide evidence of adaptation, following a human-to-poultry host transition. This has important implications for the emergence and dissemination of new pathogenic clones associated with modern agriculture.

AB - Staphylococcus aureus are globally disseminated among farmed chickens causing skeletal muscle infections, dermatitis and septicaemia. The emergence of poultry-associated lineages has involved zoonotic transmission from humans to chickens but questions remain about the specific adaptations that promote proliferation of chicken pathogens. We characterised genetic variation in a population of genome-sequenced S. aureus isolates of poultry and human origin. Genealogical analysis identified a dominant poultry-associated sequence cluster within the CC5 clonal complex. Poultry and human CC5 isolates were significantly distinct from each other and more recombination events were detected in the poultry isolates. We identified forty-four recombination events in 33 genes along the branch extending to the poultry-specific CC5 cluster, and 47 genes were found more often in CC5 poultry isolates compared to those from humans. Many of these gene sequences were common in chicken isolates from other clonal complexes suggesting horizontal gene transfer among poultry associated lineages. Consistent with functional predictions for putative poultry-associated genes, poultry isolates showed enhanced growth at 42oC and greater erythrocyte lysis on chicken blood agar in comparison with human isolates. By combining phenotype information with evolutionary analysis of staphylococcal genomes, we provide evidence of adaptation, following a human-to-poultry host transition. This has important implications for the emergence and dissemination of new pathogenic clones associated with modern agriculture.

KW - Staphylococcus

KW - Genomics

KW - Poultry infection

KW - Evolution

KW - Recombination

U2 - 10.1093/gbe/evx037

DO - 10.1093/gbe/evx037

M3 - Article

C2 - 28338786

SN - 1759-6653

VL - 9

SP - 830

EP - 842

JO - Genome Biology and Evolution

JF - Genome Biology and Evolution

IS - 4

ER -

Recombination-mediated host-adaptation by avian Staphylococcus aureus

Abstract

Keywords / Materials (for Non-textual outputs)

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Projects

Innate immunity and endemic diseases in livestock species

Cite this