Rapid evolution of virulence and drug resistance in the emerging zoonotic pathogen streptococcus suis

Matthew T. G. Holden; Heidi Hauser; Mandy Sanders; Thi Hoa Ngo; Inna Cherevach; Ann Cronin; Ian Goodhead; Karen Mungall; Michael A. Quail; Claire Price; Ester Rabbinowitsch; Sarah Sharp; Nicholas J. Croucher; Tran Bich Chieu; Nguyen Thi Hoang Mai; To Song Diep; Nguyen Tran Chinh; Michael Kehoe; James A. Leigh; Philip N. Ward; Christopher G. Dowson; Adrian M. Whatmore; Neil Chanter; Pernille Iversen; Marcelo Gottschalk; Josh D. Slater; Hilde E. Smith; Brian G. Spratt; Jianguo Xu; Changyun Ye; Stephen Bentley; Barclay G. Barrell; Constance Schultsz; Duncan J. Maskell; Julian Parkhill

doi:10.1371/journal.pone.0006072

Rapid evolution of virulence and drug resistance in the emerging zoonotic pathogen streptococcus suis

Matthew T. G. Holden^*, Heidi Hauser, Mandy Sanders, Thi Hoa Ngo, Inna Cherevach, Ann Cronin, Ian Goodhead, Karen Mungall, Michael A. Quail, Claire Price, Ester Rabbinowitsch, Sarah Sharp, Nicholas J. Croucher, Tran Bich Chieu, Nguyen Thi Hoang Mai, To Song Diep, Nguyen Tran Chinh, Michael Kehoe, James A. Leigh, Philip N. WardChristopher G. Dowson, Adrian M. Whatmore, Neil Chanter, Pernille Iversen, Marcelo Gottschalk, Josh D. Slater, Hilde E. Smith, Brian G. Spratt, Jianguo Xu, Changyun Ye, Stephen Bentley, Barclay G. Barrell, Constance Schultsz, Duncan J. Maskell, Julian Parkhill

^*Corresponding author for this work

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

Abstract

Background: Streptococcus suis is a zoonotic pathogen that infects pigs and can occasionally cause serious infections in humans. S. suis infections occur sporadically in human Europe and North America, but a recent major outbreak has been described in China with high levels of mortality. The mechanisms of S. suis pathogenesis in humans and pigs are poorly understood.

Methodology/Principal Findings: The sequencing of whole genomes of S. suis isolates provides opportunities to investigate the genetic basis of infection. Here we describe whole genome sequences of three S. suis strains from the same lineage: one from European pigs, and two from human cases from China and Vietnam. Comparative genomic analysis was used to investigate the variability of these strains. S. suis is phylogenetically distinct from other Streptococcus species for which genome sequences are currently available. Accordingly, similar to 40% of the similar to 2 Mb genome is unique in comparison to other Streptococcus species. Finer genomic comparisons within the species showed a high level of sequence conservation; virtually all of the genome is common to the S. suis strains. The only exceptions are three similar to 90 kb regions, present in the two isolates from humans, composed of integrative conjugative elements and transposons. Carried in these regions are coding sequences associated with drug resistance. In addition, small-scale sequence variation has generated pseudogenes in putative virulence and colonization factors.

Conclusions/Significance: The genomic inventories of genetically related S. suis strains, isolated from distinct hosts and diseases, exhibit high levels of conservation. However, the genomes provide evidence that horizontal gene transfer has contributed to the evolution of drug resistance.

Original language	English
Article number	e6072
Number of pages	17
Journal	PLoS One
Volume	4
Issue number	7
DOIs	https://doi.org/10.1371/journal.pone.0006072
Publication status	Published - 15 Jul 2009

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© 2009 Holden et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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Holden, M. T. G., Hauser, H., Sanders, M., Ngo, T. H., Cherevach, I., Cronin, A., Goodhead, I., Mungall, K., Quail, M. A., Price, C., Rabbinowitsch, E., Sharp, S., Croucher, N. J., Chieu, T. B., Mai, N. T. H., Diep, T. S., Chinh, N. T., Kehoe, M., Leigh, J. A., ... Parkhill, J. (2009). Rapid evolution of virulence and drug resistance in the emerging zoonotic pathogen streptococcus suis. PLoS One, 4(7), Article e6072. https://doi.org/10.1371/journal.pone.0006072

@article{e0adc00c386b442cb6160c52eed972e8,

title = "Rapid evolution of virulence and drug resistance in the emerging zoonotic pathogen streptococcus suis",

abstract = "Background: Streptococcus suis is a zoonotic pathogen that infects pigs and can occasionally cause serious infections in humans. S. suis infections occur sporadically in human Europe and North America, but a recent major outbreak has been described in China with high levels of mortality. The mechanisms of S. suis pathogenesis in humans and pigs are poorly understood.Methodology/Principal Findings: The sequencing of whole genomes of S. suis isolates provides opportunities to investigate the genetic basis of infection. Here we describe whole genome sequences of three S. suis strains from the same lineage: one from European pigs, and two from human cases from China and Vietnam. Comparative genomic analysis was used to investigate the variability of these strains. S. suis is phylogenetically distinct from other Streptococcus species for which genome sequences are currently available. Accordingly, similar to 40\% of the similar to 2 Mb genome is unique in comparison to other Streptococcus species. Finer genomic comparisons within the species showed a high level of sequence conservation; virtually all of the genome is common to the S. suis strains. The only exceptions are three similar to 90 kb regions, present in the two isolates from humans, composed of integrative conjugative elements and transposons. Carried in these regions are coding sequences associated with drug resistance. In addition, small-scale sequence variation has generated pseudogenes in putative virulence and colonization factors.Conclusions/Significance: The genomic inventories of genetically related S. suis strains, isolated from distinct hosts and diseases, exhibit high levels of conservation. However, the genomes provide evidence that horizontal gene transfer has contributed to the evolution of drug resistance.",

author = "Holden, \{Matthew T. G.\} and Heidi Hauser and Mandy Sanders and Ngo, \{Thi Hoa\} and Inna Cherevach and Ann Cronin and Ian Goodhead and Karen Mungall and Quail, \{Michael A.\} and Claire Price and Ester Rabbinowitsch and Sarah Sharp and Croucher, \{Nicholas J.\} and Chieu, \{Tran Bich\} and Mai, \{Nguyen Thi Hoang\} and Diep, \{To Song\} and Chinh, \{Nguyen Tran\} and Michael Kehoe and Leigh, \{James A.\} and Ward, \{Philip N.\} and Dowson, \{Christopher G.\} and Whatmore, \{Adrian M.\} and Neil Chanter and Pernille Iversen and Marcelo Gottschalk and Slater, \{Josh D.\} and Smith, \{Hilde E.\} and Spratt, \{Brian G.\} and Jianguo Xu and Changyun Ye and Stephen Bentley and Barrell, \{Barclay G.\} and Constance Schultsz and Maskell, \{Duncan J.\} and Julian Parkhill",

note = "This work was supported by the Wellcome Trust. ",

year = "2009",

month = jul,

day = "15",

doi = "10.1371/journal.pone.0006072",

language = "English",

volume = "4",

journal = "PLoS One",

issn = "1932-6203",

publisher = "Public Library of Science",

number = "7",

}

Holden, MTG, Hauser, H, Sanders, M, Ngo, TH, Cherevach, I, Cronin, A, Goodhead, I, Mungall, K, Quail, MA, Price, C, Rabbinowitsch, E, Sharp, S, Croucher, NJ, Chieu, TB, Mai, NTH, Diep, TS, Chinh, NT, Kehoe, M, Leigh, JA, Ward, PN, Dowson, CG, Whatmore, AM, Chanter, N, Iversen, P, Gottschalk, M, Slater, JD, Smith, HE, Spratt, BG, Xu, J, Ye, C, Bentley, S, Barrell, BG, Schultsz, C, Maskell, DJ & Parkhill, J 2009, 'Rapid evolution of virulence and drug resistance in the emerging zoonotic pathogen streptococcus suis', PLoS One, vol. 4, no. 7, e6072. https://doi.org/10.1371/journal.pone.0006072

TY - JOUR

T1 - Rapid evolution of virulence and drug resistance in the emerging zoonotic pathogen streptococcus suis

AU - Holden, Matthew T. G.

AU - Hauser, Heidi

AU - Sanders, Mandy

AU - Ngo, Thi Hoa

AU - Cherevach, Inna

AU - Cronin, Ann

AU - Goodhead, Ian

AU - Mungall, Karen

AU - Quail, Michael A.

AU - Price, Claire

AU - Rabbinowitsch, Ester

AU - Sharp, Sarah

AU - Croucher, Nicholas J.

AU - Chieu, Tran Bich

AU - Mai, Nguyen Thi Hoang

AU - Diep, To Song

AU - Chinh, Nguyen Tran

AU - Kehoe, Michael

AU - Leigh, James A.

AU - Ward, Philip N.

AU - Dowson, Christopher G.

AU - Whatmore, Adrian M.

AU - Chanter, Neil

AU - Iversen, Pernille

AU - Gottschalk, Marcelo

AU - Slater, Josh D.

AU - Smith, Hilde E.

AU - Spratt, Brian G.

AU - Xu, Jianguo

AU - Ye, Changyun

AU - Bentley, Stephen

AU - Barrell, Barclay G.

AU - Schultsz, Constance

AU - Maskell, Duncan J.

AU - Parkhill, Julian

N1 - This work was supported by the Wellcome Trust.

PY - 2009/7/15

Y1 - 2009/7/15

N2 - Background: Streptococcus suis is a zoonotic pathogen that infects pigs and can occasionally cause serious infections in humans. S. suis infections occur sporadically in human Europe and North America, but a recent major outbreak has been described in China with high levels of mortality. The mechanisms of S. suis pathogenesis in humans and pigs are poorly understood.Methodology/Principal Findings: The sequencing of whole genomes of S. suis isolates provides opportunities to investigate the genetic basis of infection. Here we describe whole genome sequences of three S. suis strains from the same lineage: one from European pigs, and two from human cases from China and Vietnam. Comparative genomic analysis was used to investigate the variability of these strains. S. suis is phylogenetically distinct from other Streptococcus species for which genome sequences are currently available. Accordingly, similar to 40% of the similar to 2 Mb genome is unique in comparison to other Streptococcus species. Finer genomic comparisons within the species showed a high level of sequence conservation; virtually all of the genome is common to the S. suis strains. The only exceptions are three similar to 90 kb regions, present in the two isolates from humans, composed of integrative conjugative elements and transposons. Carried in these regions are coding sequences associated with drug resistance. In addition, small-scale sequence variation has generated pseudogenes in putative virulence and colonization factors.Conclusions/Significance: The genomic inventories of genetically related S. suis strains, isolated from distinct hosts and diseases, exhibit high levels of conservation. However, the genomes provide evidence that horizontal gene transfer has contributed to the evolution of drug resistance.

AB - Background: Streptococcus suis is a zoonotic pathogen that infects pigs and can occasionally cause serious infections in humans. S. suis infections occur sporadically in human Europe and North America, but a recent major outbreak has been described in China with high levels of mortality. The mechanisms of S. suis pathogenesis in humans and pigs are poorly understood.Methodology/Principal Findings: The sequencing of whole genomes of S. suis isolates provides opportunities to investigate the genetic basis of infection. Here we describe whole genome sequences of three S. suis strains from the same lineage: one from European pigs, and two from human cases from China and Vietnam. Comparative genomic analysis was used to investigate the variability of these strains. S. suis is phylogenetically distinct from other Streptococcus species for which genome sequences are currently available. Accordingly, similar to 40% of the similar to 2 Mb genome is unique in comparison to other Streptococcus species. Finer genomic comparisons within the species showed a high level of sequence conservation; virtually all of the genome is common to the S. suis strains. The only exceptions are three similar to 90 kb regions, present in the two isolates from humans, composed of integrative conjugative elements and transposons. Carried in these regions are coding sequences associated with drug resistance. In addition, small-scale sequence variation has generated pseudogenes in putative virulence and colonization factors.Conclusions/Significance: The genomic inventories of genetically related S. suis strains, isolated from distinct hosts and diseases, exhibit high levels of conservation. However, the genomes provide evidence that horizontal gene transfer has contributed to the evolution of drug resistance.

UR - https://www.scopus.com/pages/publications/67650658074

U2 - 10.1371/journal.pone.0006072

DO - 10.1371/journal.pone.0006072

M3 - Article

SN - 1932-6203

VL - 4

JO - PLoS One

JF - PLoS One

IS - 7

M1 - e6072

ER -

Rapid evolution of virulence and drug resistance in the emerging zoonotic pathogen streptococcus suis

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