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

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Holden, Matthew T. G., Hauser, Heidi, Sanders, Mandy, Ngo, Thi Hoa, Cherevach, Inna, Cronin, Ann, Goodhead, Ian, Mungall, Karen, Quail, Michael A., Price, Claire et al.
. (2009) Rapid evolution of virulence and drug resistance in the emerging zoonotic pathogen Streptococcus suis. PLOS One, Vol.4 (No.7). ISSN 1932-6203

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Official URL: http://dx.doi.org/10.1371/journal.pone.0006072

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, ,40% of the ,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 ,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.

Item Type: Journal Article
Subjects: Q Science > QR Microbiology
Divisions: Faculty of Science > Life Sciences (2010- ) > Biological Sciences ( -2010)
Library of Congress Subject Headings (LCSH): Streptococcus -- Genetics, Zoonoses -- Genetic aspects, Streptococcal infections -- Pathogenesis, Drug resistance in microorganisms
Journal or Publication Title: PLOS One
Publisher: Public Library of Science
ISSN: 1932-6203
Date: 15 July 2009
Volume: Vol.4
Number: No.7
Identification Number: 10.1371/journal.pone.0006072
Status: Peer Reviewed
Access rights to Published version: Open Access
Funder: Wellcome Trust (London, England)
References: 1. Gottschalk M, Segura M, Xu J (2007) Streptococcus suis infections in humans: the Chinese experience and the situation in North America. Anim Health Res Rev 8: 29–45. 2. Perch B, Kristjansen P, Skadhauge K (1968) Group R streptococci pathogenic for man. Two cases of meningitis and one fatal case of sepsis. Acta Pathol Microbiol Scand 74: 69–76. 3. Mai NT, Hoa NT, Nga TV, Linh LD, Chau TT, et al. (2008) Streptococcus suis meningitis in adults in Vietnam. Clin Infect Dis 46: 659–667. 4. Nghia HD, Hoa NT, Linh le D, Campbell J, Diep TS, et al. (2008) Human case of Streptococcus suis serotype 16 infection. Emerg Infect Dis 14: 155–157. 5. Yu H, Jing H, Chen Z, Zheng H, Zhu X, et al. (2006) Human Streptococcus suis outbreak, Sichuan, China. Emerg Infect Dis 12: 914–920. 6. Sriskandan S, Slater JD (2006) Invasive disease and toxic shock due to zoonotic Streptococcus suis: an emerging infection in the East? PLoS Medicine 3: e187. 7. Chen C, Tang J, Dong W, Wang C, Feng Y, et al. (2007) A glimpse of streptococcal toxic shock syndrome from comparative genomics of S. suis 2 Chinese isolates. PLoS ONE 2: e315. 8. Ye C, Zhu X, Jing H, Du H, Segura M, et al. (2006) Streptococcus suis sequence type 7 outbreak, Sichuan, China. Emerg Infect Dis 12: 1203–1208. 9. Clifton-Hadley FA (1981) Studies of Streptococcus suis type 2 infection in pigs: University of Cambridge. 10. King SJ, Leigh JA, Heath PJ, Luque I, Tarradas C, et al. (2002) Development of a multilocus sequence typing scheme for the pig pathogen Streptococcus suis: identification of virulent clones and potential capsular serotype exchange. J Clin Microbiol 40: 3671–3680. 11. Ye C, Bai X, Zhang J, Jing H, Zheng H, et al. (2008) Spread of Streptococcus suis sequence type 7, China. Emerg Infect Dis 14: 787–791. 12. Ning Z, Cox AJ, Mullikin JC (2001) SSAHA: a fast search method for large DNA databases. Genome Res 11: 1725–1729. 13. Dear S, Durbin R, Hillier L, Marth G, Thierry-Mieg J, et al. (1998) Sequence assembly with CAFTOOLS. Genome Res 8: 260–267. 14. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic Local Alignment Search Tool. Journal of Molecular Biology 215: 403–410. 15. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, et al. (2000) Artemis: sequence visualization and annotation. Bioinformatics 16: 944–945. 16. Frishman D, Mironov A, Mewes HW, Gelfand M (1998) Combining diverse evidence for gene recognition in completely sequenced bacterial genomes. Nucleic Acids Research 26: 2941–2947. 17. Delcher AL, Harmon D, Kasif S, White O, Salzberg SL (1999) Improved microbial gene identification with GLIMMER. Nucleic Acids Research 27: 4636–4641. 18. Larsen TS, Krogh A (2003) EasyGene–a prokaryotic gene finder that ranks ORFs by statistical significance. BMC Bioinformatics 4: 21. 19. Pearson WR, Lipman DJ (1988) Improved Tools for Biological Sequence Comparison. Proceedings of the National Academy of Sciences of the United States of America 85: 2444–2448. 20. Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, et al. (2002) The Pfam Protein Families Database. Nucleic Acids Research 30: 276–280. 21. Falquet L, Pagni M, Bucher P, Hulo N, Sigrist CJA, et al. (2002) The PROSITE database, its status in 2002. Nucleic Acids Research 30: 235–238. 22. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. Journal of Molecular Biology 305: 567–580. 23. Nielsen H, Engelbrecht J, Brunak S, vonHeijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Engineering 10: 1–6. 24. Lowe TM, Eddy SR (1997) tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Research 25: 955–964. 25. Griffiths-Jones S, Bateman A, Marshall M, Khanna A, Eddy SR (2003) Rfam: an RNA family database. Nucleic Acids Research 31: 439–441. 26. Carver TJ, Rutherford K, Berriman M, Rajandream MA, Barrell B, et al. (2005) ACT: the Artemis comparison tool. Bioinformatics 21: 3422–3423. 27. Kurtz S, Phillippy A, Delcher AL, SmootM, ShumwayM, et al. (2004) Versatile and open software for comparing large genomes. Genome Biol 5: R12. 28. Didelot X, Falush D (2007) Inference of bacterial microevolution using multilocus sequence data. Genetics 175: 1251–1266. 29. Holden MT, Scott A, Cherevach I, Chillingworth T, Churcher C, et al. (2007) Complete genome of acute rheumatic fever-associated serotype M5 Streptococcus pyogenes strain manfredo. J Bacteriol 189: 1473–1477. 30. Holden MT, Heather Z, Paillot R, Steward KF, Webb K, et al. (2009) Genomic evidence for the evolution of Streptococcus equi: host restriction, increased virulence, and genetic exchange with human pathogens. PLoS Pathogens 5: e1000346. 31. Ward PN, Holden MTG, Leigh JA, Lennard N, Bignell A, et al. (2009) Evidence for niche adaptation in the genome of the bovine pathogen Streptococcus uberis. BMC Genomics 10: 54. 32. Bolotin A, Quinquis B, Renault P, Sorokin A, Ehrlich SD, et al. (2004) Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus. Nat Biotechnol 22: 1554–1558. 33. Tettelin H, Nelson KE, Paulsen IT, Eisen JA, Read TD, et al. (2001) Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293: 498–506. 34. Xu P, Alves JM, Kitten T, Brown A, Chen Z, et al. (2007) Genome of the opportunistic pathogen Streptococcus sanguinis. J Bacteriol 189: 3166–3175. 35. Ajdic D, McShan WM, McLaughlin RE, Savic G, Chang J, et al. (2002) Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen. Proc Natl Acad Sci U S A 99: 14434–14439. 36. Glaser P, Rusniok C, Buchrieser C, Chevalier F, Frangeul L, et al. (2002) Genome sequence of Streptococcus agalactiae, a pathogen causing invasive neonatal disease. Mol Microbiol 45: 1499–1513. 37. Vickerman MM, Iobst S, Jesionowski AM, Gill SR (2007) Genome-wide transcriptional changes in Streptococcus gordonii in response to competence signaling peptide. J Bacteriol 189: 7799–7807. 38. Bolotin A, Wincker P, Mauger S, Jaillon O, Malarme K, et al. (2001) The complete genome sequence of the lactic acid bacterium Lactococcus lactis ssp. lactis IL1403. Genome Res 11: 731–753. 39. Wilm A, Higgins DG, Notredame C (2008) R-Coffee: a method for multiple alignment of non-coding RNA. Nucleic Acids Res 36: e52. 40. Galtier N, Gouy M, Gautier C (1996) SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12: 543–548. 41. Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294: 2310–2314. 42. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574. 43. Smith HE, Damman M, van der Velde J, Wagenaar F, Wisselink HJ, et al. (1999) Identification and characterization of the cps locus of Streptococcus suis serotype 2: the capsule protects against phagocytosis and is an important virulence factor. Infect Immun 67: 1750–1756. 44. Smith HE, de Vries R, van’t Slot R, Smits MA (2000) The cps locus of Streptococcus suis serotype 2: genetic determinant for the synthesis of sialic acid. Microb Pathog 29: 127–134. 45. Elliott SD, Tai JY (1978) The type-specific polysaccharides of Streptococcus suis. J Exp Med 148: 1699–1704. 46. Higgins R, Gottschalk M (2001) Distribution of Streptococcus suis capsular types in 2000. Can Vet J 42: 223. 47. Wisselink HJ, Smith HE, Stockhofe-Zurwieden N, Peperkamp K, Vecht U (2000) Distribution of capsular types and production of muramidase-released protein (MRP) and extracellular factor (EF) of Streptococcus suis strains isolated from diseased pigs in seven European countries. Vet Microbiol 74: 237–248. 48. Arends JP, Zanen HC (1988) Meningitis caused by Streptococcus suis in humans. Rev Infect Dis 10: 131–137. 49. Charland N, Harel J, Kobisch M, Lacasse S, Gottschalk M (1998) Streptococcus suis serotype 2 mutants deficient in capsular expression. Microbiology 144(Pt 2): 325–332. 50. Jobin MC, Gottschalk M, Grenier D (2006) Upregulation of prostaglandin E2 and matrix metalloproteinase 9 production by human macrophage-like cells: synergistic effect of capsular material and cell wall from Streptococcus suis. Microb Pathog 40: 29–34. 51. Tsukioka Y, Yamashita Y, Nakano Y, Oho T, Koga T (1997) Identification of a fourth gene involved in dTDP-rhamnose synthesis in Streptococcus mutans. Journal of Bacteriology 179: 4411–4414. 52. Tsukioka Y, Yamashita Y, Oho T, Nakano Y, Koga T (1997) Biological function of the dTDP-rhamnose synthesis pathway in Streptococcus mutans. Journal of Bacteriology 179: 1126–1134. 53. Yamashita Y, Tsukioka Y, Nakano Y, Tomihisa K, Oho T, et al. (1998) Biological functions of UDP-glucose synthesis in Streptococcus mutans. Microbiology 144(Pt 5): 1235–1245. 54. Yamashita Y, Shibata Y, Nakano Y, Tsuda H, Kido N, et al. (1999) A novel gene required for rhamnose-glucose polysaccharide synthesis in Streptococcus mutans. Journal of Bacteriology 181: 6556–6559. 55. Shibata Y, Yamashita Y, Ozaki K, Nakano Y, Koga T (2002) Expression and characterization of streptococcal rgp genes required for rhamnan synthesis in Escherichia coli. Infect Immun 70: 2891–2898. 56. Ozaki K, Shibata Y, Yamashita Y, Nakano Y, Tsuda H, et al. (2002) A novel mechanism for glucose side-chain formation in rhamnose-glucose polysaccharide synthesis. FEBS Lett 532: 159–163. 57. Broadbent JR, McMahon DJ, Welker DL, Oberg CJ, Moineau S (2003) Biochemistry, genetics, and applications of exopolysaccharide production in Streptococcus thermophilus: a review. J Dairy Sci 86: 407–423. 58. Soell M, Lett E, Holveck F, Scholler M, Wachsmann D, et al. (1995) Activation of human monocytes by streptococcal rhamnose glucose polymers is mediated by CD14 antigen, and mannan binding protein inhibits TNF-alpha release. J Immunol 154: 851–860. 59. Martin V, Kleschyov AL, Klein JP, Beretz A (1997) Induction of nitric oxide production by polyosides from the cell walls of Streptococcus mutans OMZ 175, a gram-positive bacterium, in the rat aorta. Infect Immun 65: 2074–2079. 60. Tsuda H, Yamashita Y, Toyoshima K, Yamaguchi N, Oho T, et al. (2000) Role of serotype-specific polysaccharide in the resistance of Streptococcus mutans to phagocytosis by human polymorphonuclear leukocytes. Infect Immun 68: 644–650. 61. Koedel U, Bernatowicz A, Paul R, Frei K, Fontana A, et al. (1995) Experimental pneumococcal meningitis: cerebrovascular alterations, brain edema, and meningeal inflammation are linked to the production of nitric oxide. Ann Neurol 37: 313–323. 62. Kornelisse RF, Hoekman K, Visser JJ, Hop WC, Huijmans JG, et al. (1996) The role of nitric oxide in bacterial meningitis in children. Journal of Infectious Diseases 174: 120–126. 63. Dominguez-Punaro MC, Segura M, Plante MM, Lacouture S, Rivest S, et al. (2007) Streptococcus suis serotype 2, an important swine and human pathogen, induces strong systemic and cerebral inflammatory responses in a mouse model of infection. J Immunol 179: 1842–1854. 64. Planet PJ, Kachlany SC, DeSalle R, Figurski DH (2001) Phylogeny of genes for secretion NTPases: identification of the widespread tadA subfamily and development of a diagnostic key for gene classification. Proceedings of the National Academy of Sciences of the United States of America 98: 2503–2508. 65. Jacobs AA, Loeffen PL, van den Berg AJ, Storm PK (1994) Identification, purification, and characterization of a thiol-activated hemolysin (suilysin) of Streptococcus suis. Infect Immun 62: 1742–1748. 66. King SJ, Heath PJ, Luque I, Tarradas C, Dowson CG, et al. (2001) Distribution and genetic diversity of suilysin in Streptococcus suis isolated from different diseases of pigs and characterization of the genetic basis of suilysin absence. Infect Immun 69: 7572–7582. 67. Billington SJ, Jost BH, Songer JG (2000) Thiol-activated cytolysins: structure, function and role in pathogenesis. FEMS Microbiol Lett 182: 197–205. 68. Jacobs AA, van den Berg AJ, Loeffen PL (1996) Protection of experimentally infected pigs by suilysin, the thiol-activated haemolysin of Streptococcus suis. Vet Rec 139: 225–228. 69. Allen AG, Bolitho S, Lindsay H, Khan S, Bryant C, et al. (2001) Generation and characterization of a defined mutant of Streptococcus suis lacking suilysin. Infect Immun 69: 2732–2735. 70. Osaki M, Takamatsu D, Shimoji Y, Sekizaki T (2002) Characterization of Streptococcus suis genes encoding proteins homologous to sortase of gram-positive bacteria. Journal of Bacteriology 184: 971–982. 71. Fittipaldi N, Gottschalk M, Vanier G, Daigle F, Harel J (2007) Use of selective capture of transcribed sequences to identify genes preferentially expressed by Streptococcus suis upon interaction with porcine brain microvascular endothelial cells. Appl Environ Microbiol 73: 4359–4364. 72. Oggioni MR, Memmi G, Maggi T, Chiavolini D, Iannelli F, et al. (2003) Pneumococcal zinc metalloproteinase ZmpC cleaves human matrix metalloproteinase 9 and is a virulence factor in experimental pneumonia. Mol Microbiol 49: 795–805. 73. Poulsen K, Reinholdt J, Kilian M (1996) Characterization of the Streptococcus pneumoniae immunoglobulin A1 protease gene (iga) and its translation product. Infect Immun 64: 3957–3966. 74. Novak R, Charpentier E, Braun JS, Park E, Murti S, et al. (2000) Extracellular targeting of choline-binding proteins in Streptococcus pneumoniae by a zinc metalloprotease. Mol Microbiol 36: 366–376. 75. Paul R, Lorenzl S, Koedel U, Sporer B, Vogel U, et al. (1998) Matrix metalloproteinases contribute to the blood-brain barrier disruption during bacterial meningitis. Ann Neurol 44: 592–600. 76. Leppert D, Leib SL, Grygar C, Miller KM, Schaad UB, et al. (2000) Matrix metalloproteinase (MMP)-8 and MMP-9 in cerebrospinal fluid during bacterial meningitis: association with blood-brain barrier damage and neurological sequelae. Clin Infect Dis 31: 80–84. 77. Weiser JN, Bae D, Fasching C, Scamurra RW, Ratner AJ, et al. (2003) Antibody-enhanced pneumococcal adherence requires IgA1 protease. Proceedings of the National Academy of Sciences of the United States of America 100: 4215–4220. 78. Smith HE, Vecht U, Gielkens AL, Smits MA (1992) Cloning and nucleotide sequence of the gene encoding the 136-kilodalton surface protein (muramidasereleased protein) of Streptococcus suis type 2. Infect Immun 60: 2361–2367. 79. Smith HE, Reek FH, Vecht U, Gielkens AL, Smits MA (1993) Repeats in an extracellular protein of weakly pathogenic strains of Streptococcus suis type 2 are absent in pathogenic strains. Infect Immun 61: 3318–3326. 80. Gottschalk M, Lebrun A, Wisselink H, Dubreuil JD, Smith H, et al. (1998) Production of virulence-related proteins by Canadian strains of Streptococcus suis capsular type 2. Can J Vet Res 62: 75–79. 81. Smith HE, Vecht U, Wisselink HJ, Stockhofe-Zurwieden N, Biermann Y, et al. (1996) Mutants of Streptococcus suis types 1 and 2 impaired in expression of muramidase-released protein and extracellular protein induce disease in newborn germfree pigs. Infect Immun 64: 4409–4412. 82. Baums CG, Kaim U, Fulde M, Ramachandran G, Goethe R, et al. (2006) Identification of a novel virulence determinant with serum opacification activity in Streptococcus suis. Infect Immun 74: 6154–6162. 83. Dramsi S, Caliot E, Bonne I, Guadagnini S, Prevost MC, et al. (2006) Assembly and role of pili in group B streptococci. Mol Microbiol 60: 1401–1413. 84. Takamatsu D, Nishino H, Ishiji T, Ishii J, Osaki M, et al. (2009) Genetic organization and preferential distribution of putative pilus gene clusters in Streptococcus suis. Vet Microbiol, in press. 85. Lei B, DeLeo FR, Hoe NP, Graham MR, Mackie SM, et al. (2001) Evasion of human innate and acquired immunity by a bacterial homolog of CD11b that inhibits opsonophagocytosis. Nat Med 7: 1298–1305. 86. von Pawel-Rammingen U, Johansson BP, Bjorck L (2002) IdeS, a novel streptococcal cysteine proteinase with unique specificity for immunoglobulin G. EMBO Journal
URI: http://wrap.warwick.ac.uk/id/eprint/4424

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