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Volume 170, Issue 9

Variation in bacterial pathotype is consistent with the sit-and-wait hypothesis Open Access

Abstract

The sit-and-wait hypothesis predicts that bacteria can become more virulent when they survive and transmit outside of their hosts due to circumventing the costs of host mortality. While this hypothesis is largely supported theoretically and through comparative analysis, experimental validation is limited. Here we test this hypothesis in , an opportunistic zoonotic pig pathogen, where a pathogenic ecotype proliferated during the change to intensive pig farming that amplifies opportunities for fomite transmission. We show in an environmental survival experiment that pathogenic ecotypes survive for longer than commensal ecotypes, despite similar rates of decline. The presence of a polysaccharide capsule has no consistent effect on survival. Our findings suggest that extended survival in the food chain may augment the zoonotic capability of . Moreover, eliminating the long-term environmental survival of bacteria could be a strategy that will both enhance infection control and curtail the evolution of virulence.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): environmental survival , evolution of virulence , indirect transmission , Pharaoh’s curse , resource allocation hypothesis , Streptococcus suis and zoonosis
Funding
This study was supported by the:
  • Royal Society (Award 109385/Z/15/Z)
    • Principle Award Recipient: LucyWeinert
  • Wellcome Trust (Award 109385/Z/15/Z)
    • Principle Award Recipient: LucyWeinert
© 2024 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2024-09-17
2024-10-14
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References

  1. Anderson RM, May RM. Coevolution of hosts and parasites. Parasitology 1982; 85:411–426 [View Article] [PubMed]
     [Google Scholar]
  2. Ewald PW. Host-parasite relations, vectors, and the evolution of disease severity. Annu Rev Ecol Syst 1983; 14:465–485 [View Article]
     [Google Scholar]
  3. Ewald PW. Evolution of Infectious Disease Oxford University Press; 1994 p 309
     [Google Scholar]
  4. Ewald PW. Chapter 11 - Pathogen-induced cycling of outbreak insect populations. In Barbosa P, Schultz JC. eds Insect Outbreaks San Diego: Academic Press; 1987 pp 269–286 [View Article]
     [Google Scholar]
  5. Ewald PW. Evolution of virulence. Infect Dis Clin North Am 2004; 18:1–15 [View Article] [PubMed]
     [Google Scholar]
  6. Walther BA, Ewald PW. Pathogen survival in the external environment and the evolution of virulence. Biol Rev Camb Philos Soc 2004; 79:849–869 [View Article] [PubMed]
     [Google Scholar]
  7. Gandon S. The curse of the pharaoh hypothesis. Proc Biol Sci 1998; 265:1545–1552 [View Article] [PubMed]
     [Google Scholar]
  8. Bonhoeffer S, Lenski RE, Ebert D. The curse of the pharaoh: the evolution of virulence in pathogens with long living propagules. Proc Biol Sci 1996; 263:715–721 [View Article] [PubMed]
     [Google Scholar]
  9. Alizon S, Hurford A, Mideo N, Van Baalen M. Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J Evol Biol 2009; 22:245–259 [View Article] [PubMed]
     [Google Scholar]
  10. Roche B, Drake JM, Rohani P. The curse of the Pharaoh revisited: evolutionary bi-stability in environmentally transmitted pathogens. Ecol Lett 2011; 14:569–575 [View Article] [PubMed]
     [Google Scholar]
  11. Ferenci T. Trade-off mechanisms shaping the diversity of bacteria. Trends Microbiol 2016; 24:209–223 [View Article] [PubMed]
     [Google Scholar]
  12. Wang L, Liu Z, Dai S, Yan J, Wise MJ. The sit-and-wait hypothesis in bacterial pathogens: a theoretical study of durability and virulence. Front Microbiol 2017; 8:2167 [View Article]
     [Google Scholar]
  13. Rafaluk-Mohr C. The relationship between parasite virulence and environmental persistence: a meta-analysis. Parasitology 2019; 146:897–902 [View Article] [PubMed]
     [Google Scholar]
  14. Sundberg L-R, Kunttu HMT, Valtonen ET. Starvation can diversify the population structure and virulence strategies of an environmentally transmitting fish pathogen. BMC Microbiol 2014; 14:67 [View Article] [PubMed]
     [Google Scholar]
  15. Berthelot-Hérault F, Gottschalk M, Labbé A, Cariolet R, Kobisch M. Experimental airborne transmission of Streptococcus suis capsular type 2 in pigs. Vet Microbiol 2001; 82:69–80 [View Article] [PubMed]
     [Google Scholar]
  16. Vela AI, Goyache J, Tarradas C, Luque I, Mateos A et al. Analysis of genetic diversity of Streptococcus suis clinical isolates from pigs in Spain by pulsed-field gel electrophoresis. J Clin Microbiol 2003; 41:2498–2502 [View Article] [PubMed]
     [Google Scholar]
  17. Murray GGR, Hossain ASMM, Miller EL, Bruchmann S, Balmer AJ et al. The emergence and diversification of a zoonotic pathogen from within the microbiota of intensively farmed pigs. Proc Natl Acad Sci U S A 2023; 120:e2307773120 [View Article] [PubMed]
     [Google Scholar]
  18. Murray GGR, Charlesworth J, Miller EL, Casey MJ, Lloyd CT et al. Genome reduction is associated with bacterial pathogenicity across different scales of temporal and ecological divergence. Mol Biol Evol 2021; 38:1570–1579 [View Article] [PubMed]
     [Google Scholar]
  19. Dee SA. The survival of Streptococcus suis on farm and veterinary equipment. J Swine Health Prod 1993; 1:17–20
     [Google Scholar]
  20. Helke KL, Ezell PC, Duran-Struuck R, Swindle MM. Chapter 16 - Biology and diseases of Swine. In Fox JG, Anderson LC, Otto GM, Pritchett-Corning KR, Whary MT. eds Laboratory Animal Medicine, 3rd edn. American College of Laboratory Animal Medicine. Boston: Academic Press; 2015 pp 695–769 [View Article]
     [Google Scholar]
  21. Clifton-Hadley FA, Enright MR. Factors affecting the survival of Streptococcus suis type 2. Vet Rec 1984; 114:584–586 [View Article] [PubMed]
     [Google Scholar]
  22. Clifton-Hadley FA, Alexander TJ. The carrier site and carrier rate of Streptococcus suis type II in pigs. Vet Rec 1980; 107:40–41 [View Article] [PubMed]
     [Google Scholar]
  23. Keonam K, Nam NH, Saksangawong C, Sringam P, Saipan P et al. Prevalence of Streptococcus suis serotype 2 isolated from pigs: a systematic review and meta-analysis. Vet World 2024; 17:233–244 [View Article] [PubMed]
     [Google Scholar]
  24. Perch B, Kristjansen P, Skadhauge K. Group R streptococci pathogenic for man. Two cases of meningitis and one fatal case of sepsis. Acta Pathol Microbiol Scand 1968; 74:69–76 [PubMed]
     [Google Scholar]
  25. Staats JJ, Feder I, Okwumabua O, Chengappa MM. Streptococcus suis: past and present. Vet Res Commun 1997; 21:381–407 [View Article] [PubMed]
     [Google Scholar]
  26. Brown SP, Cornforth DM, Mideo N. Evolution of virulence in opportunistic pathogens: generalism, plasticity, and control. Trends Microbiol 2012; 20:336–342 [View Article] [PubMed]
     [Google Scholar]
  27. 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 [View Article] [PubMed]
     [Google Scholar]
  28. Zafar MA, Hamaguchi S, Zangari T, Cammer M, Weiser JN. Capsule type and amount affect shedding and transmission of Streptococcus pneumoniae. mBio 2017; 8:e00989-17 [View Article] [PubMed]
     [Google Scholar]
  29. Jones BA, Grace D, Kock R, Alonso S, Rushton J et al. Zoonosis emergence linked to agricultural intensification and environmental change. Proc Natl Acad Sci USA 2013; 110:8399–8404 [View Article]
     [Google Scholar]
  30. Drew TW. The emergence and evolution of swine viral diseases: to what extend have husbandry systems and global trade contributed to their distribution and diversity?. Rev Sci Tech OIE 2011; 30:95–106 [View Article]
     [Google Scholar]
  31. Graham JP, Leibler JH, Price LB, Otte JM, Pfeiffer DU et al. The animal-human interface and infectious disease in industrial food animal production: rethinking biosecurity and biocontainment. Public Health Rep 2008; 123:282–299 [View Article] [PubMed]
     [Google Scholar]
  32. Tonkin-Hill G, MacAlasdair N, Ruis C, Weimann A, Horesh G et al. Producing polished prokaryotic pangenomes with the Panaroo pipeline. Genome Biol 2020; 21:180 [View Article] [PubMed]
     [Google Scholar]
  33. Paradis E, Claude J, Strimmer K. APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics 2004; 20:289–290 [View Article] [PubMed]
     [Google Scholar]
  34. Athey TBT, Teatero S, Lacouture S, Takamatsu D, Gottschalk M et al. Determining Streptococcus suis serotype from short-read whole-genome sequencing data. BMC Microbiol 2016; 16:162 [View Article] [PubMed]
     [Google Scholar]
  35. Tipton KA, Chin C-Y, Farokhyfar M, Weiss DS, Rather PN. Role of capsule in resistance to disinfectants, host antimicrobials, and desiccation in Acinetobacter baumannii. Antimicrob Agents Chemother 2018; 62:01188-18 [View Article]
     [Google Scholar]
  36. Hamaguchi S, Zafar MA, Cammer M, Weiser JN. Capsule prolongs survival of Streptococcus pneumoniae during starvation. Infect Immun 2018; 86:e00802-17 [View Article] [PubMed]
     [Google Scholar]
  37. Brazeau C, Gottschalk M, Vincelette S, Martineau-Doizé B. In vitro phagocytosis and survival of Streptococcus suis capsular type 2 inside murine macrophages. Microbiology 1996; 142:1231–1237 [View Article] [PubMed]
     [Google Scholar]
  38. Lewis K. Persister cells. Annu Rev Microbiol 2010; 64:357–372 [View Article] [PubMed]
     [Google Scholar]
  39. Willenborg J, Willms D, Bertram R, Goethe R, Valentin-Weigand P. Characterization of multi-drug tolerant persister cells in Streptococcus suis. BMC Microbiol 2014; 14:1–9 [View Article] [PubMed]
     [Google Scholar]
  40. Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S. Bacterial persistence as a phenotypic switch. Science 2004; 305:1622–1625 [View Article] [PubMed]
     [Google Scholar]
  41. Amato SM, Orman MA, Brynildsen MP. Metabolic control of persister formation in Escherichia coli. Mol Cell 2013; 50:475–487 [View Article] [PubMed]
     [Google Scholar]
  42. Vega NM, Allison KR, Khalil AS, Collins JJ. Signaling-mediated bacterial persister formation. Nat Chem Biol 2012; 8:431–433 [View Article] [PubMed]
     [Google Scholar]
  43. Tram G, Jen FE, Phillips ZN, Timms J, Husna A-U et al. Streptococcus suis encodes multiple allelic variants of a phase-variable type III DNA methyltransferase, ModS, that control distinct phasevarions. mSphere 2021; 6:e00069-21 [View Article] [PubMed]
     [Google Scholar]
  44. Atack JM, Weinert LA, Tucker AW, Husna AU, Wileman TM et al. Streptococcus suis contains multiple phase-variable methyltransferases that show a discrete lineage distribution. Nucleic Acids Res 2018; 46:11466–11476 [View Article]
     [Google Scholar]
  45. Jäger HC, McKinley TJ, Wood JLN, Pearce GP, Williamson S et al. Factors associated with pleurisy in pigs: a case-control analysis of slaughter pig data for England and Wales. PLoS One 2012; 7:e29655 [View Article] [PubMed]
     [Google Scholar]
  46. Dong X, Chao Y, Zhou Y, Zhou R, Zhang W et al. The global emergence of a novel Streptococcus suis clade associated with human infections. EMBO Mol Med 2021; 13:e13810 [View Article] [PubMed]
     [Google Scholar]
/content/journal/micro/10.1099/mic.0.001500
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Variation in bacterial pathotype is consistent with the sit-and-wait hypothesis
Microbiology 170, 001500 (2024); https://doi.org/10.1099/mic.0.001500
/content/journal/micro/10.1099/mic.0.001500
/content/journal/micro/10.1099/mic.0.001500
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