Skip to content
1887

Microbial Genomics logo Microbial Genomics

Volume 10, Issue 12

infection on European farms is associated with an altered tonsil microbiome and resistome Open Access

Abstract

is a Gram-positive opportunistic pathogen causing systemic disease in piglets around weaning age. The factors predisposing to disease are not known. We hypothesized that the tonsillar microbiota might influence disease risk via colonization resistance and/or co-infections. We conducted a cross-sectional case–control study within outbreak farms complemented by selective longitudinal sampling and comparison with control farms without disease occurrence. We found a small but significant difference in tonsil microbiota composition between case and control piglets (=45+45). Variants of putative commensal taxa, including , were reduced in abundance in case piglets compared to asymptomatic controls. Case piglets had higher relative abundances of , and uncultured and species. Piglets developing disease post-weaning had reduced alpha diversity pre-weaning. Despite case–control pairs receiving equal antimicrobial treatment, case piglets had a higher abundance of antimicrobial resistance genes conferring resistance to antimicrobial classes used to treat . This might be an adaption of disease-associated strains to frequent antimicrobial treatment.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): AMR , colonization resistance , S. suis carriage , S. suis infection , Streptococcus suis and tonsil microbiome
Funding
This study was supported by the:
  • Horizon 2020 Framework Programme (Award 727966)
    • Principal Award Recipient: JerryM Wells
© 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.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.001334
2024-12-19
2026-01-24

Metrics

Loading full text...

Full text loading...

/deliver/fulltext/mgen/10/12/mgen001334.html?itemId=/content/journal/mgen/10.1099/mgen.0.001334&mimeType=html&fmt=ahah

References

  1. Gottschalk M, Segura M. The pathogenesis of the meningitis caused by Streptococcus suis: the unresolved questions. Vet Microbiol 2000; 76:259–272 [View Article] [PubMed]
     [Google Scholar]
  2. Lun Z-R, Wang Q-P, Chen X-G, Li A-X, Zhu X-Q. Streptococcus suis: an emerging zoonotic pathogen. Lancet Infect Dis 2007; 7:201–209 [View Article] [PubMed]
     [Google Scholar]
  3. Neila-Ibáñez C, Casal J, Hennig-Pauka I, Stockhofe-Zurwieden N, Gottschalk M et al. Stochastic assessment of the economic impact of Streptococcus suis-associated disease in German, Dutch and Spanish swine farms. Front Vet Sci 2021; 8:676002 [View Article] [PubMed]
     [Google Scholar]
  4. Vötsch D, Willenborg M, Weldearegay YB, Valentin-Weigand P. Streptococcus suis - The “Two Faces” of a pathobiont in the porcine respiratory tract. Front Microbiol 2018; 9:480 [View Article] [PubMed]
     [Google Scholar]
  5. Aarestrup FM, Rasmussen SR, Artursson K, Jensen NE. Trends in the resistance to antimicrobial agents of Streptococcus suis isolates from Denmark and Sweden. Vet Microbiol 1998; 63:71–80 [View Article] [PubMed]
     [Google Scholar]
  6. Uruén C, García C, Fraile L, Tommassen J, Arenas J. How Streptococcus suis escapes antibiotic treatments. Vet Res 2022; 53:91 [View Article] [PubMed]
     [Google Scholar]
  7. Hadjirin NF, Miller EL, Murray GGR, Yen PLK, Phuc HD et al. Large-scale genomic analysis of antimicrobial resistance in the zoonotic pathogen Streptococcus suis. BMC Biol 2021; 19:191 [View Article] [PubMed]
     [Google Scholar]
  8. Huang J, Ma J, Shang K, Hu X, Liang Y et al. Evolution and diversity of the antimicrobial resistance associated mobilome in Streptococcus suis: a probable mobile genetic elements reservoir for other streptococci. Front Cell Infect Microbiol 2016; 6:118 [View Article] [PubMed]
     [Google Scholar]
  9. Arends JP, Hartwig N, Rudolphy M, Zanen HC. Carrier rate of Streptococcus suis capsular type 2 in palatine tonsils of slaughtered pigs. J Clin Microbiol 1984; 20:945–947 [View Article] [PubMed]
     [Google Scholar]
  10. 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]
  11. Lowe BA, Marsh TL, Isaacs-Cosgrove N, Kirkwood RN, Kiupel M et al. Defining the “core microbiome” of the microbial communities in the tonsils of healthy pigs. BMC Microbiol 2012; 12:20 [View Article] [PubMed]
     [Google Scholar]
  12. Murase K, Watanabe T, Arai S, Kim H, Tohya M et al. Characterization of pig saliva as the major natural habitat of Streptococcus suis by analyzing oral, fecal, vaginal, and environmental microbiota. PLoS One 2019; 14:e0215983 [View Article] [PubMed]
     [Google Scholar]
  13. Kernaghan S, Bujold AR, MacInnes JI. The microbiome of the soft palate of swine. Anim Health Res Rev 2012; 13:110–120 [View Article] [PubMed]
     [Google Scholar]
  14. Liang Z, Wu H, Bian C, Chen H, Shen Y et al. The antimicrobial systems of Streptococcus suis promote niche competition in pig tonsils. Virulence 2022; 13:781–793 [View Article] [PubMed]
     [Google Scholar]
  15. Pena Cortes LC, LeVeque RM, Funk J, Marsh TL, Mulks MH. Development of the tonsillar microbiome in pigs from newborn through weaning. BMC Microbiol 2018; 18:35 [View Article] [PubMed]
     [Google Scholar]
  16. Pena Cortes LC, LeVeque RM, Funk JA, Marsh TL, Mulks MH. Development of the tonsil microbiome in pigs and effects of stress on the microbiome. Front Vet Sci 2018; 5:220 [View Article] [PubMed]
     [Google Scholar]
  17. Fredriksen S, Guan X, Boekhorst J, Molist F, van Baarlen P et al. Environmental and maternal factors shaping tonsillar microbiota development in piglets. BMC Microbiol 2022; 22:224 [View Article] [PubMed]
     [Google Scholar]
  18. Niazy M, Hill S, Nadeem K, Ricker N, Farzan A. Compositional analysis of the tonsil microbiota in relationship to Streptococcus suis disease in nursery pigs in Ontario. Anim Microbiome 2022; 4:10 [View Article] [PubMed]
     [Google Scholar]
  19. Gaiser R, Ferrando M, Oddo A, Pereira M, Guan X et al. A mammalian commensal of the oropharyngeal cavity produces antibiotic and antiviral valinomycin in vivo. Res Square 2021 [View Article]
     [Google Scholar]
  20. Mathieu-Denoncourt A, Letendre C, Auger J-P, Segura M, Aragon V et al. Limited interactions between Streptococcus suis and Haemophilus parasuis in in vitro co-infection studies. Pathogens 2018; 7:7 [View Article] [PubMed]
     [Google Scholar]
  21. Obradovic MR, Segura M, Segalés J, Gottschalk M. Review of the speculative role of co-infections in Streptococcus suis-associated diseases in pigs. Vet Res 2021; 52:49 [View Article] [PubMed]
     [Google Scholar]
  22. Thanawongnuwech R, Brown GB, Halbur PG, Roth JA, Royer RL et al. Pathogenesis of porcine reproductive and respiratory syndrome virus-induced increase in susceptibility to Streptococcus suis infection. Vet Pathol 2000; 37:143–152 [View Article] [PubMed]
     [Google Scholar]
  23. Segura M, Calzas C, Grenier D, Gottschalk M. Initial steps of the pathogenesis of the infection caused by Streptococcus suis: fighting against nonspecific defenses. FEBS Lett 2016; 590:3772–3799 [View Article] [PubMed]
     [Google Scholar]
  24. Roodsant TJ, Van Der Putten BCL, Tamminga SM, Schultsz C, Van Der Ark KCH. Identification of Streptococcus suis putative zoonotic virulence factors: a systematic review and genomic meta-analysis. Virulence 2021; 12:2787–2797 [View Article] [PubMed]
     [Google Scholar]
  25. Weinert LA, Chaudhuri RR, Wang J, Peters SE, Corander J et al. Genomic signatures of human and animal disease in the zoonotic pathogen Streptococcus suis. Nat Commun 2015; 6:6740 [View Article] [PubMed]
     [Google Scholar]
  26. Wileman TM, Weinert LA, Howell KJ, Wang J, Peters SE et al. Pathotyping the zoonotic pathogen Streptococcus suis: novel genetic markers to differentiate invasive disease-associated isolates from non-disease-associated isolates from England and Wales. J Clin Microbiol 2019; 57:e01712-18
     [Google Scholar]
  27. Fredriksen S, Ruijten SDE, Murray GGR, Juanpere-Borràs M, Baarlen P et al. Transcriptomics in serum and culture medium reveal shared and differential gene regulation in pathogenic and commensal Streptococcus suis. Microb Genom 2023; 9:000992
     [Google Scholar]
  28. Murray GGR, Hossain ASMdM, 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 USA 2023; 120:e2307773120 [View Article]
     [Google Scholar]
  29. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
     [Google Scholar]
  30. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
     [Google Scholar]
  31. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
     [Google Scholar]
  32. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 2011; 17:10 [View Article]
     [Google Scholar]
  33. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA et al. DADA2: high-resolution sample inference from illumina amplicon data. Nat Methods 2016; 13:581–583 [View Article] [PubMed]
     [Google Scholar]
  34. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 2013; 41:D590–D596 [View Article] [PubMed]
     [Google Scholar]
  35. Steinegger M, Söding J. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat Biotechnol 2017; 35:1026–1028 [View Article] [PubMed]
     [Google Scholar]
  36. McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 2013; 8:e61217 [View Article] [PubMed]
     [Google Scholar]
  37. Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH et al. The vegan package. Commun Ecol Package 2007; 10:631–637
     [Google Scholar]
  38. Wood DE, Lu J, Langmead B. Improved metagenomic analysis with Kraken 2. Genome Biol 2019; 20:257 [View Article] [PubMed]
     [Google Scholar]
  39. Uritskiy GV, DiRuggiero J, Taylor J. MetaWRAP-a flexible pipeline for genome-resolved metagenomic data analysis. Microbiome 2018; 6:158 [View Article] [PubMed]
     [Google Scholar]
  40. Chaumeil P-A, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 2020; 36:1925–1927 [View Article]
     [Google Scholar]
  41. Bortolaia V, Kaas RS, Ruppe E, Roberts MC, Schwarz S et al. ResFinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother 2020; 75:3491–3500 [View Article] [PubMed]
     [Google Scholar]
  42. Wirbel J, Zych K, Essex M, Karcher N, Kartal E et al. Microbiome meta-analysis and cross-disease comparison enabled by the SIAMCAT machine learning toolbox. Genome Biol 2021; 22:93
     [Google Scholar]
  43. Opriessnig T, Giménez-Lirola LG, Halbur PG. Polymicrobial respiratory disease in pigs. Anim Health Res Rev 2011; 12:133–148 [View Article] [PubMed]
     [Google Scholar]
  44. De Witte C, Demeyere K, De Bruyckere S, Taminiau B, Daube G et al. Characterization of the non-glandular gastric region microbiota in Helicobacter suis-infected versus non-infected pigs identifies a potential role for Fusobacterium gastrosuis in gastric ulceration. Vet Res 2019; 50:39 [View Article] [PubMed]
     [Google Scholar]
  45. Wolff B, Boutin S, Lorenz H-M, Ueffing H, Dalpke A et al. FRI0698 prevotella and alloprevotella species characterize the oral microbiome of early rheumatoid arthritis. Ann Rheum Dis 2017754 [View Article]
     [Google Scholar]
  46. Fredriksen S, de Warle S, van Baarlen P, Boekhorst J, Wells JM. Resistome expansion in disease-associated human gut microbiomes. Microbiome 2023; 11:166 [View Article] [PubMed]
     [Google Scholar]
  47. de Oliveira OI, Ng DYK, van Baarlen P, Stegger M, Andersen PS et al. Comparative genomics of rothia species reveals diversity in novel biosynthetic gene clusters and ecological adaptation to different eukaryotic hosts and host niches. Microb Genom 2022; 8:000854
     [Google Scholar]
  48. Correa-Fiz F, Gonçalves Dos Santos JM, Illas F, Aragon V. Antimicrobial removal on piglets promotes health and higher bacterial diversity in the nasal microbiota. Sci Rep 2019; 9:6545 [View Article] [PubMed]
     [Google Scholar]
  49. Hall CW, Mah T-F. Molecular mechanisms of biofilm-based antibiotic resistance and tolerance in pathogenic bacteria. FEMS Microbiol Rev 2017; 41:276–301 [View Article] [PubMed]
     [Google Scholar]
  50. Ricker N, Trachsel J, Colgan P, Jones J, Choi J et al. Toward antibiotic stewardship: route of antibiotic administration impacts the microbiota and resistance gene diversity in swine feces. Front Vet Sci 2020; 7:255 [View Article] [PubMed]
     [Google Scholar]
  51. Zhang L, Huang Y, Zhou Y, Buckley T, Wang HH. Antibiotic administration routes significantly influence the levels of antibiotic resistance in gut microbiota. Antimicrob Agents Chemother 2013; 57:3659–3666 [View Article]
     [Google Scholar]
  52. Law K, Lozinski B, Torres I, Davison S, Hilbrands A et al. Disinfection of maternal environments is associated with piglet microbiome composition from birth to weaning. mSphere 2021; 6:e00663–21 [View Article]
     [Google Scholar]
  53. Holman DB, Gzyl KE, Mou KT, Allen HK. Weaning age and its effect on the development of the swine gut microbiome and resistome. mSystems 2021; 6:e0068221 [View Article] [PubMed]
     [Google Scholar]
  54. Choudhury R, Middelkoop A, Boekhorst J, Gerrits WJJ, Kemp B et al. Early life feeding accelerates gut microbiome maturation and suppresses acute post-weaning stress in piglets. Environ Microbiol 2021; 23:7201–7213 [View Article] [PubMed]
     [Google Scholar]
  55. Vo N, Tsai TC, Maxwell C, Carbonero F. Early exposure to agricultural soil accelerates the maturation of the early-life pig gut microbiota. Anaerobe 2017; 45:31–39 [View Article] [PubMed]
     [Google Scholar]
  56. Megahed A, Zeineldin M, Evans K, Maradiaga N, Blair B et al. Impacts of environmental complexity on respiratory and gut microbiome community structure and diversity in growing pigs. Sci Rep 2019; 9:13773 [View Article] [PubMed]
     [Google Scholar]
  57. Munk P, Knudsen BE, Lukjancenko O, Duarte ASR, Van Gompel L et al. Abundance and diversity of the faecal resistome in slaughter pigs and broilers in nine European countries. Nat Microbiol 2018; 3:898–908 [View Article] [PubMed]
     [Google Scholar]
  58. Mencía-Ares O, Cabrera-Rubio R, Cobo-Díaz JF, Álvarez-Ordóñez A, Gómez-García M et al. Antimicrobial use and production system shape the fecal, environmental, and slurry resistomes of pig farms. Microbiome 2020; 8:164 [View Article] [PubMed]
     [Google Scholar]
  59. Zou G, Zhou J, Xiao R, Zhang L, Cheng Y et al. Effects of environmental and management-associated factors on prevalence and diversity of Streptococcus suis in clinically healthy pig herds in china and the United Kingdom. Appl Environ Microbiol 2018; 84:e02590-17 [View Article] [PubMed]
     [Google Scholar]
  60. Correa-Fiz F, Blanco-Fuertes M, Navas MJ, Lacasta A, Bishop RP et al. Comparative analysis of the fecal microbiota from different species of domesticated and wild suids. Sci Rep 2019; 9:13616 [View Article] [PubMed]
     [Google Scholar]
  61. Huang J, Zhang W, Fan R, Liu Z, Huang T et al. Composition and functional diversity of fecal bacterial community of wild boar, commercial pig and domestic native pig as revealed by 16S rRNA gene sequencing. Arch Microbiol 2020; 202:843–857 [View Article] [PubMed]
     [Google Scholar]
  62. Petrelli S, Buglione M, Maselli V, Troiano C, Larson G et al. Population genomic, olfactory, dietary, and gut microbiota analyses demonstrate the unique evolutionary trajectory of feral pigs. Mol Ecol 2022; 31:220–237 [View Article] [PubMed]
     [Google Scholar]
  63. Correa-Fiz F, Fraile L, Aragon V. Piglet nasal microbiota at weaning may influence the development of Glässer’s disease during the rearing period. BMC Genomics 2016; 17:404 [View Article] [PubMed]
     [Google Scholar]
  64. Corsaut L, Misener M, Canning P, Beauchamp G, Gottschalk M et al. Field study on the immunological response and protective effect of a licensed autogenous vaccine to control Streptococcus suis infections in post-weaned piglets. Vaccines 2020; 8:384 [View Article] [PubMed]
     [Google Scholar]
  65. Curtis J, Bourne FJ. Half-lives of immunoglobulins IgG, IgA and IgM in the serum of new-born pigs. Immunology 1973; 24:147–155 [PubMed]
     [Google Scholar]
  66. Morris CR, Gardner IA, Hietala SK, Carpenter TE, Anderson RJ et al. Persistence of passively acquired antibodies to Mycoplasma hyopneumoniae in a swine herd. Prevent Vet Med 1994; 21:29–41 [View Article]
     [Google Scholar]
  67. Procházka Z, Fránek M, Krejĉí J. Duration of the persistence of 131I-labelled colostral and serum IgG in the blood of newborn piglets. Zentralblatt für Veterinärmedizin Reihe B 1979; 26:366–370 [View Article]
     [Google Scholar]
  68. Vandeputte J, Too HL, Ng FK, Chen C, Chai KK et al. Adsorption of colostral antibodies against classical swine fever, persistence of maternal antibodies, and effect on response to vaccination in baby pigs. Am J Vet Res 2001; 62:1805–1811 [View Article] [PubMed]
     [Google Scholar]
  69. Vigre H, Ersbøll AK, Sørensen V. Decay of acquired colostral antibodies to Actinobacillus pleuropneumoniae in pigs. J Vet Med Ser B 2003; 50:430–435 [View Article]
     [Google Scholar]
/content/journal/mgen/10.1099/mgen.0.001334
Loading
Streptococcus suis infection on European farms is associated with an altered tonsil microbiome and resistome
M Gen 10, 001334 (2024); https://doi.org/10.1099/mgen.0.001334
/content/journal/mgen/10.1099/mgen.0.001334
/content/journal/mgen/10.1099/mgen.0.001334
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An error occurred
Approval was partially successful, following selected items could not be processed due to error