1887

Microbial Genomics logo

Volume 6, Issue 8

Comparative genome analysis of isolated from domestic pigs and wild boars suggests host adaptation and selective pressure from the use of antibiotics Open Access

Abstract

The disease erysipelas caused by (ER) is a major concern in pig production. In the present study the genomes of ER from pigs (=87), wild boars (=71) and other sources (=85) were compared in terms of whole-genome SNP variation, accessory genome content and the presence of genetic antibiotic resistance determinants. The aim was to investigate if genetic features among ER were associated with isolate origin in order to better estimate the risk of transmission of porcine-adapted strains from wild boars to free-range pigs and to increase our understanding of the evolution of ER. Pigs and wild boars carried isolates representing all ER clades, but clade one only occurred in healthy wild boars and healthy pigs. Several accessory genes or gene variants were found to be significantly associated with the pig and wild boar hosts, with genes predicted to encode cell wall-associated or extracellular proteins overrepresented. Gene variants associated with serovar determination and capsule production in serovars known to be pathogenic for pigs were found to be significantly associated with pigs as hosts. In total, 30 % of investigated pig isolates but only 6 % of wild boar isolates carried resistance genes, most commonly (tetracycline) and (E) together with (B) (lincosamides, pleuromutilin and streptogramin A). The incidence of variably present genes including resistance determinants was weakly linked to phylogeny, indicating that host adaptation in ER has evolved multiple times in diverse lineages mediated by recombination and the acquisition of mobile genetic elements. The presented results support the occurrence of host-adapted ER strains, but they do not indicate frequent transmission between wild boars and domestic pigs. This article contains data hosted by Microreact.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): antibiotic resistance , erysipelas , genomics , molecular epidemiology , pan-genome analysis and wildlife
Funding
This study was supported by the:
  • Animal Health and Welfare ERA-Net (ANIHWA) (Award 221-2015-1895, 5192-00004B)
    • Principle Award Recipient: Helena Eriksson
© 2020 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000412
2020-07-31
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/mgen/6/8/mgen000412.html?itemId=/content/journal/mgen/10.1099/mgen.0.000412&mimeType=html&fmt=ahah

References

  1. Wang Q, Chang BJ, Riley TV. Erysipelothrix rhusiopathiae. Vet Microbiol 2010; 140:405–417 [View Article][PubMed]
     [Google Scholar]
  2. Wood RL. Survival of Erysipelothrix rhusiopathiae in soil under various environmental conditions. Cornell Vet 1973; 63:390–410[PubMed]
     [Google Scholar]
  3. Opriessnig T, Wood RL. Erysipelas. In Ramirez A, Schwartz K, Stevenson G. (editors) Diseases of Swine John Wiley & Sons; 2012 pp 750–757
     [Google Scholar]
  4. Colavita G, Vergara A, Ianieri A. Deferment of slaughtering in swine affected by cutaneous erysipelas. Meat Sci 2006; 72:203–205 [View Article][PubMed]
     [Google Scholar]
  5. Bender J, Madson D. What's the real cost of swine erysipelas?. National Hog Farmer 2009
     [Google Scholar]
  6. Reboli AC, Farrar WE. Erysipelothrix rhusiopathiae: an occupational pathogen. Clin Microbiol Rev 1989; 2:354–359 [View Article][PubMed]
     [Google Scholar]
  7. Massei G, Kindberg J, Licoppe A, Gačić D, Šprem N et al. Wild boar populations up, numbers of hunters down? A review of trends and implications for Europe. Pest Manag Sci 2015; 71:492–500 [View Article][PubMed]
     [Google Scholar]
  8. Boadella M, Ruiz-Fons JF, Vicente J, Martín M, Segalés J et al. Seroprevalence evolution of selected pathogens in Iberian wild boar. Transbound Emerg Dis 2012; 59:395–404 [View Article][PubMed]
     [Google Scholar]
  9. Malmsten A, Magnusson U, Ruiz-Fons F, González-Barrio D, Dalin A-M. A Serologic Survey of Pathogens in Wild Boar (Sus Scrofa) in Sweden. J Wildl Dis 2018; 54:229–237 [View Article][PubMed]
     [Google Scholar]
  10. Shimizu T, Okamoto C, Aoki H, Harada K, Kataoka Y et al. Serological surveillance for antibodies against Erysipelothrix species in wild boar and deer in Japan. Jpn J Vet Res 2016; 64:91–94[PubMed]
     [Google Scholar]
  11. Shimoji Y, Osaki M, Ogawa Y, Shiraiwa K, Nishikawa S et al. Wild boars: a potential source of Erysipelothrix rhusiopathiae infection in Japan. Microbiol Immunol 2019; 63:465–468 [View Article][PubMed]
     [Google Scholar]
  12. Risco D, Llario PF, Velarde R, García WL, Benítez JM et al. Outbreak of swine erysipelas in a semi-intensive wild boar farm in Spain. Transbound Emerg Dis 2011; 58:445–450 [View Article][PubMed]
     [Google Scholar]
  13. Yamamoto K, Kijima M, Takahashi T, Yoshimura H, Tani O et al. Serovar, pathogenicity and antimicrobial susceptibility of Erysipelothrix rhusiopathiae isolates from farmed wild boars (Sus scrofa) affected with septicemic erysipelas in Japan. Res Vet Sci 1999; 67:301–303 [View Article][PubMed]
     [Google Scholar]
  14. Wiedenbeck J, Cohan FM. Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. FEMS Microbiol Rev 2011; 35:957–976 [View Article][PubMed]
     [Google Scholar]
  15. Hottes AK, Freddolino PL, Khare A, Donnell ZN, Liu JC et al. Bacterial adaptation through loss of function. PLoS Genet 2013; 9:e1003617 [View Article][PubMed]
     [Google Scholar]
  16. Navarre WW, Schneewind O. Surface proteins of Gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 1999; 63:174–229 [View Article][PubMed]
     [Google Scholar]
  17. Forde T, Biek R, Zadoks R, Workentine ML, De Buck J et al. Genomic analysis of the multi-host pathogen Erysipelothrix rhusiopathiae reveals extensive recombination as well as the existence of three generalist clades with wide geographic distribution. BMC Genomics 2016; 17:461 [View Article][PubMed]
     [Google Scholar]
  18. Kwok AHY, Li Y, Jiang J, Jiang P, Leung FC. Complete genome assembly and characterization of an outbreak strain of the causative agent of swine erysipelas--Erysipelothrix rhusiopathiae SY1027. BMC Microbiol 2014; 14:176 [View Article][PubMed]
     [Google Scholar]
  19. Ogawa Y, Ooka T, Shi F, Ogura Y, Nakayama K et al. The genome of Erysipelothrix rhusiopathiae, the causative agent of swine erysipelas, reveals new insights into the evolution of Firmicutes and the organism's intracellular adaptations. J Bacteriol 2011; 193:2959–2971 [View Article][PubMed]
     [Google Scholar]
  20. Ogawa Y, Shiraiwa K, Ogura Y, Ooka T, Nishikawa S et al. Clonal lineages of Erysipelothrix rhusiopathiae responsible for acute swine erysipelas in Japan identified by using genome-wide single-nucleotide polymorphism analysis. Appl Environ Microbiol 2017; 83: [View Article][PubMed]
     [Google Scholar]
  21. Tang H-bo, Xie J, Wang L, Liu F, Wu J. Complete genome sequence of Erysipelothrix rhusiopathiae strain GXBY-1 isolated from acute swine erysipelas outbreaks in South China. Genom Data 2016; 8:70–71 [View Article]
     [Google Scholar]
  22. Zoric M, Eriksson H, Wallgren P, Söderlund R. Prevalence and Genomic Characteristics of Erysipelothrix Rhusiopathiae in Healthy Swedish Pigs. 11th European Symposium of Porcine Health Management Utrecht: The Netherlands; 2019
     [Google Scholar]
  23. Söderlund R, Hakhverdyan M, Aspán A, Jansson E. Genome analysis provides insights into the epidemiology of infection with Flavobacterium psychrophilum among farmed salmonid fish in Sweden. Microb Genom 2018; 4: [View Article]
     [Google Scholar]
  24. Cingolani P, Platts A, Wang le L, Coon M, Nguyen T. Wang L, et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 2012; 6:80–92
     [Google Scholar]
  25. 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]
     [Google Scholar]
  26. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 2014; 9:e112963 [View Article]
     [Google Scholar]
  27. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article]
     [Google Scholar]
  28. Brynildsrud O, Bohlin J, Scheffer L, Eldholm V. Rapid scoring of genes in microbial pan-genome-wide association studies with Scoary. Genome Biol 2016; 17:238 [View Article]
     [Google Scholar]
  29. Hochberg Y, Benjamini Y. More powerful procedures for multiple significance testing. Stat Med 1990; 9:811–818 [View Article]
     [Google Scholar]
  30. Stothard P. The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques 2000; 28:1102–1104 [View Article]
     [Google Scholar]
  31. NY Y, Wagner JR, Laird MR, Melli G, Rey S et al. PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics 2010; 26:1608–1615
     [Google Scholar]
  32. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 2012; 67:2640–2644 [View Article]
     [Google Scholar]
  33. Shen HG, Bender JS, Opriessnig T. Identification of surface protective antigen (spa) types in Erysipelothrix reference strains and diagnostic samples by spa multiplex real-time and conventional PCR assays. J Appl Microbiol 2010; 109:1227–1233 [View Article]
     [Google Scholar]
  34. Shiraiwa K, Ogawa Y, Nishikawa S, Eguchi M, Shimoji Y. Identification of serovar 1A, 1B, 2, and 5 strains of Erysipelothrix rhusiopathiae by a conventional gel-based PCR. Vet Microbiol 2018; 225:101–104 [View Article]
     [Google Scholar]
  35. Argimón S, Abudahab K, Goater RJE, Fedosejev A, Bhai J et al. Microreact: visualizing and sharing data for genomic epidemiology and phylogeography. Microb Genom 2016; 2:e000093 [View Article]
     [Google Scholar]
  36. Ogawa Y, Shiraiwa K, Nishikawa S, Eguchi M, Shimoji Y. Identification of the Chromosomal Region Essential for Serovar-Specific Antigen and Virulence of Serovar 1 and 2 Strains of Erysipelothrix rhusiopathiae . Infect Immun 2018; 86: [View Article]
     [Google Scholar]
  37. Janßen T, Voss M, Kühl M, Semmler T, Philipp H-C et al. A combinational approach of multilocus sequence typing and other molecular typing methods in unravelling the epidemiology of Erysipelothrix rhusiopathiae strains from poultry and mammals. Vet Res 2015; 46:84 [View Article]
     [Google Scholar]
  38. Roberts AP, Mullany P. Tn 916 -like genetic elements: a diverse group of modular mobile elements conferring antibiotic resistance. FEMS Microbiol Rev 2011; 35:856–871 [View Article]
     [Google Scholar]
  39. Yamamoto K, Sasaki Y, Ogikubo Y, Noguchi N, Sasatsu M et al. Identification of the Tetracycline Resistance Gene, tet(M), in Erysipelothrix rhusiopathiae. J Vet Med B Infect Dis Vet Public Health 2001; 48:293–301 [View Article]
     [Google Scholar]
  40. Zhang A, Xu C, Wang H, Lei C, Liu B et al. Presence and new genetic environment of pleuromutilin–lincosamide–streptogramin A resistance gene lsa(E) in Erysipelothrix rhusiopathiae of swine origin. Vet Microbiol 2015; 177:162–167 [View Article]
     [Google Scholar]
  41. De Briyne N, Atkinson J, Borriello SP, Pokludová L. Antibiotics used most commonly to treat animals in Europe. Vet Rec 2014; 175:325 [View Article]
     [Google Scholar]
  42. van Duijkeren E, Greko C, Pringle M, Baptiste KE, Catry B et al. Pleuromutilins: use in food-producing animals in the European Union, development of resistance and impact on human and animal health. J Antimicrob Chemother 2014; 69:2022–2031 [View Article]
     [Google Scholar]
  43. Scornec H, Bellanger X, Guilloteau H, Groshenry G, Merlin C. Inducibility of Tn916 conjugative transfer in Enterococcus faecalis by subinhibitory concentrations of ribosome-targeting antibiotics. J Antimicrob Chemother 2017; 72:2722–2728 [View Article]
     [Google Scholar]
  44. European database of sales of veterinary antimicrobial agents: European medicines Agency. https://bi.ema.europa.eu/analyticsSOAP/saw.dll?PortalPages
  45. Yazdankhah S, Rudi K, Bernhoft A. Zinc and copper in animal feed – development of resistance and co-resistance to antimicrobial agents in bacteria of animal origin. Microb Ecol Health Dis 2014; 25: [View Article]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000412
Loading
Comparative genome analysis of Erysipelothrix rhusiopathiae isolated from domestic pigs and wild boars suggests host adaptation and selective pressure from the use of antibiotics
M Gen 6, e000412 (2020); https://doi.org/10.1099/mgen.0.000412
/content/journal/mgen/10.1099/mgen.0.000412
/content/journal/mgen/10.1099/mgen.0.000412
Loading

Data & Media loading...

Supplements

Supplementary material 1

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