1887

Abstract

The porcine pathogen Streptococcus suis colonizes the upper respiratory tracts of pigs, potentially causing septicaemia, meningitis and death, thus placing a severe burden on the agricultural industry worldwide. It is also a zoonotic pathogen that is known to cause systemic infections and meningitis in humans. Understanding how S. suis colonizes and interacts with its hosts is relevant for future strategies of drug and vaccine development. As with other Gram-positive bacteria, S. suis utilizes enzymes known as sortases to attach specific proteins bearing cell wall sorting signals to its surface, where they can play a role in host–pathogen interactions. The surface proteins of bacteria are often important in adhesion to and invasion of host cells. In this study, markerless in-frame deletion mutants of the housekeeping sortase srtA and the two pilus-associated sortases, srtB and srtF, were generated and their importance in S. suis infections was investigated. We found that all three of these sortases are essential to disease in pigs, concluding that their cognate-sorted proteins may also be useful in protecting pigs against infection.

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2018-12-13
2019-10-22
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References

  1. Feng Y, Zhang H, Wu Z, Wang S, Cao M et al. Streptococcus suis infection: an emerging/reemerging challenge of bacterial infectious diseases?. Virulence 2014;5:477–497 [CrossRef][PubMed]
    [Google Scholar]
  2. Goyette-Desjardins G, Auger JP, Xu J, Segura M, Gottschalk M. Streptococcus suis, an important pig pathogen and emerging zoonotic agent-an update on the worldwide distribution based on serotyping and sequence typing. Emerg Microbes Infect 2014;3:e45 [CrossRef][PubMed]
    [Google Scholar]
  3. Wangkaew S, Chaiwarith R, Tharavichitkul P, Supparatpinyo K. Streptococcus suis infection: a series of 41 cases from Chiang Mai University Hospital. J Infect 2006;52:455–460 [CrossRef][PubMed]
    [Google Scholar]
  4. Ngo TH, Tran TB, Tran TT, Nguyen VD, Campbell J et al. Slaughterhouse pigs are a major reservoir of Streptococcus suis serotype 2 capable of causing human infection in southern Vietnam. PLoS One 2011;6:e17943 [CrossRef][PubMed]
    [Google Scholar]
  5. Charland N, Harel J, Kobisch M, Lacasse S, Gottschalk M. Streptococcus suis serotype 2 mutants deficient in capsular expression. Microbiology 1998;144:325–332 [CrossRef][PubMed]
    [Google Scholar]
  6. Feng Y, Cao M, Shi J, Zhang H, Hu D et al. Attenuation of Streptococcus suis virulence by the alteration of bacterial surface architecture. Sci Rep 2012;2:710 [CrossRef][PubMed]
    [Google Scholar]
  7. Smith HE, Damman M, van der Velde J, Wagenaar F, Wisselink HJ et al. 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 1999;67:1750–1756[PubMed]
    [Google Scholar]
  8. Pian Y, Gan S, Wang S, Guo J, Wang P et al. Fhb, a novel factor H-binding surface protein, contributes to the antiphagocytic ability and virulence of Streptococcus suis. Infect Immun 2012;80:2402–2413 [CrossRef][PubMed]
    [Google Scholar]
  9. Tang Y, Zhang X, Yin Y, Hardwidge PR, Fang W. Streptococcus suis type 2 SSU0587 protein is a beta-galactosidase that contributes to bacterial adhesion but not to virulence in mice. J Vet Med Sci 2014;76:1055–1059 [CrossRef][PubMed]
    [Google Scholar]
  10. Schneewind O, Missiakas D. Sec-secretion and sortase-mediated anchoring of proteins in Gram-positive bacteria. Biochim Biophys Acta 2014;1843:1687–1697 [CrossRef][PubMed]
    [Google Scholar]
  11. Spirig T, Weiner EM, Clubb RT. Sortase enzymes in Gram-positive bacteria. Mol Microbiol 2011;82:1044–1059 [CrossRef][PubMed]
    [Google Scholar]
  12. Osaki M, Takamatsu D, Shimoji Y, Sekizaki T. Allelic variation in srtAs of Streptococcus suis strains. FEMS Microbiol Lett 2003;219:195–201 [CrossRef][PubMed]
    [Google Scholar]
  13. Wang C, Li M, Feng Y, Zheng F, Dong Y et al. The involvement of sortase A in high virulence of STSS-causing Streptococcus suis serotype 2. Arch Microbiol 2009;191:23–33 [CrossRef][PubMed]
    [Google Scholar]
  14. Vanier G, Sekizaki T, Domínguez-Punaro MC, Esgleas M, Osaki M et al. Disruption of srtA gene in Streptococcus suis results in decreased interactions with endothelial cells and extracellular matrix proteins. Vet Microbiol 2008;127:417–424 [CrossRef][PubMed]
    [Google Scholar]
  15. Shaik MM, Maccagni A, Tourcier G, di Guilmi AM, Dessen A. Structural basis of pilus anchoring by the ancillary pilin RrgC of Streptococcus pneumoniae. J Biol Chem 2014;289:16988–16997 [CrossRef][PubMed]
    [Google Scholar]
  16. Okura M, Osaki M, Fittipaldi N, Gottschalk M, Sekizaki T et al. The minor pilin subunit Sgp2 is necessary for assembly of the pilus encoded by the srtG cluster of Streptococcus suis. J Bacteriol 2011;193:822–831 [CrossRef][PubMed]
    [Google Scholar]
  17. Osaki M, Takamatsu D, Shimoji Y, Sekizaki T. Characterization of Streptococcus suis genes encoding proteins homologous to sortase of Gram-positive bacteria. J Bacteriol 2002;184:971–982 [CrossRef][PubMed]
    [Google Scholar]
  18. Takamatsu D, Nishino H, Ishiji T, Ishii J, Osaki M et al. Genetic organization and preferential distribution of putative pilus gene clusters in Streptococcus suis. Vet Microbiol 2009;138:132–139 [CrossRef][PubMed]
    [Google Scholar]
  19. Shao J, Zhang W, Wu Z, Lu C. The truncated major pilin subunit Sbp2 of the srtBCD pilus cluster still contributes to Streptococcus suis pathogenesis in the absence of pilus shaft. Curr Microbiol 2014;69:703–707 [CrossRef][PubMed]
    [Google Scholar]
  20. Fittipaldi N, Takamatsu D, de La Cruz Domínguez-Punaro M, Lecours MP, Montpetit D et al. Mutations in the gene encoding the ancillary pilin subunit of the Streptococcus suis srtF cluster result in pili formed by the major subunit only. PLoS One 2010;5:e8426 [CrossRef][PubMed]
    [Google Scholar]
  21. Takamatsu D, Osaki M, Sekizaki T. Construction and characterization of Streptococcus suis-Escherichia coli shuttle cloning vectors. Plasmid 2001;45:101–113 [CrossRef][PubMed]
    [Google Scholar]
  22. Faulds-Pain A, Wren BW. Improved bacterial mutagenesis by high-frequency allele exchange, demonstrated in Clostridium difficile and Streptococcus suis. Appl Environ Microbiol 2013;79:4768–4771 [CrossRef][PubMed]
    [Google Scholar]
  23. Sanchez CJ, Kumar N, Lizcano A, Shivshankar P, Dunning Hotopp JC et al. Streptococcus pneumoniae in biofilms are unable to cause invasive disease due to altered virulence determinant production. PLoS One 2011;6:e28738 [CrossRef][PubMed]
    [Google Scholar]
  24. Moscoso M, García E, López R. Biofilm formation by Streptococcus pneumoniae: role of choline, extracellular DNA, and capsular polysaccharide in microbial accretion. J Bacteriol 2006;188:7785–7795 [CrossRef][PubMed]
    [Google Scholar]
  25. Wang Y, Zhang W, Wu Z, Lu C. Reduced virulence is an important characteristic of biofilm infection of Streptococcus suis. FEMS Microbiol Lett 2011;316:36–43 [CrossRef][PubMed]
    [Google Scholar]
  26. Manetti AG, Zingaretti C, Falugi F, Capo S, Bombaci M et al. Streptococcus pyogenes pili promote pharyngeal cell adhesion and biofilm formation. Mol Microbiol 2007;64:968–983 [CrossRef][PubMed]
    [Google Scholar]
  27. Velikova N, Kavanagh K, Wells JM. Evaluation of Galleria mellonella larvae for studying the virulence of Streptococcus suis. BMC Microbiol 2016;16:291 [CrossRef][PubMed]
    [Google Scholar]
  28. Fälker S, Nelson AL, Morfeldt E, Jonas K, Hultenby K et al. Sortase-mediated assembly and surface topology of adhesive pneumococcal pili. Mol Microbiol 2008;70:595–607 [CrossRef][PubMed]
    [Google Scholar]
  29. Lemieux J, Woody S, Camilli A. Roles of the sortases of Streptococcus pneumoniae in assembly of the RlrA pilus. J Bacteriol 2008;190:6002–6013 [CrossRef][PubMed]
    [Google Scholar]
  30. Barnett TC, Patel AR, Scott JR. A novel sortase, SrtC2, from Streptococcus pyogenes anchors a surface protein containing a QVPTGV motif to the cell wall. J Bacteriol 2004;186:5865–5875 [CrossRef][PubMed]
    [Google Scholar]
  31. van Sorge NM, Cole JN, Kuipers K, Henningham A, Aziz RK et al. The classical lancefield antigen of group a Streptococcus is a virulence determinant with implications for vaccine design. Cell Host Microbe 2014;15:729–740 [CrossRef][PubMed]
    [Google Scholar]
  32. Segura M, Fittipaldi N, Calzas C, Gottschalk M. Critical Streptococcus suis virulence factors: Are they all really critical?. Trends Microbiol 2017;25:585–599 [CrossRef][PubMed]
    [Google Scholar]
  33. Holden MT, Hauser H, Sanders M, Ngo TH, Cherevach I et al. Rapid evolution of virulence and drug resistance in the emerging zoonotic pathogen Streptococcus suis. PLoS One 2009;4:e6072 [CrossRef][PubMed]
    [Google Scholar]
  34. Heap JT, Pennington OJ, Cartman ST, Minton NP. A modular system for Clostridium shuttle plasmids. J Microbiol Methods 2009;78:79–85 [CrossRef][PubMed]
    [Google Scholar]
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