Folia Microbiologica

, Volume 63, Issue 1, pp 17–22 | Cite as

Trueperella pyogenes isolated from a brain abscess of an adult roebuck (Capreolus capreolus)

  • Jörn-Peter Wickhorst
  • Abdulwahed Ahmed Hassan
  • Omar Hashim Sheet
  • Tobias Eisenberg
  • Osama Sammra
  • Mazen Alssahen
  • Christoph Lämmler
  • Ellen Prenger-Berninghoff
  • Michael Zschöck
  • Markus Timke
  • Amir Abdulmawjood
Original Article

Abstract

The present study was designed to characterize phenotypically and genotypically a Trueperella pyogenes strain isolated from a brain abscess of an adult roebuck (Capreolus capreolus). The species identity could be confirmed by phenotypical investigations, by MALDI-TOF MS analysis, and by sequencing the 16S ribosomal RNA (rRNA) gene, the 16S–23S rRNA intergenic spacer region (ISR); by sequencing the target genes rpoB, gap, and tuf; and by detection of T. pyogenes chaperonin-encoding gene cpn60 with a previously developed loop-mediated isothermal amplification (LAMP) assay. The T. pyogenes strain could additionally be characterized by PCR-mediated amplification of several known and putative virulence factor-encoding genes which revealed the presence of the genes plo encoding pyolysin and nanH and nanP encoding neuraminidases; the genes fimA, fimC, and fimE encoding the fimbrial subunits FimA, FimC, and FimE; and the gene cbpA encoding collagen-binding protein CbpA. The present data give a detailed characterization of a T. pyogenes strain isolated from a brain abscess of a roebuck. However, the route of infection of the roebuck remains unclear.

References

  1. Abdulmawjood A, Wickhorst J, Sammra O, Lämmler C, Foster G, Wragg PN, Prenger-Berninghoff E, Klein G (2015) Development of a loop-mediated isothermal amplification (LAMP) assay for rapid and sensitive identification of Arcanobacterium pluranimalium. Mol Cell Probes 29:468–472CrossRefPubMedGoogle Scholar
  2. Abdulmawjood A, Wickhorst J, Hashim O, Sammra O, Hassan AA, Alssahen M, Lämmler C, Prenger-Berninghoff E, Klein G (2016) Application of a loop-mediated isothermal amplification (LAMP) assay for molecular identification of Trueperella pyogenes isolated from various origins. Mol Cell Probes 30:205–210CrossRefPubMedGoogle Scholar
  3. Belser EH, Cohen BS, Keeler SP, Killmaster CH, Bowers JW, Miller KV (2015) Epethelial presence of Trueperella pyogenes predicts site-level presence of cranial abscess disease in white-tailed deer (Odocoileus virginianus). PLoS One 10(3):1371CrossRefGoogle Scholar
  4. Billington SJ, Jost BH, Cuevas WA, Bright KR, Songer JG (1997) The Arcanobacterium (Actinomyces) pyogenes hemolysin, pyolysin, is a novel member of the thiol-activated cytolysin family. J Bacteriol 179:6100–6106CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bizzini A, Jaton K, Romo D, Bille J, Prod’hom G, Greub G (2011) Matrix-assisted laser desorption ionization-time of flight mass spectrometry as an alternative to 16S rRNA gene sequencing for identification of difficult-to-identify bacterial strains. J Clin Microbiol 49:693–696CrossRefPubMedPubMedCentralGoogle Scholar
  6. Cohen BS, Belser EH, Killmaster CH, Bowers JW, Irwin BJ, Yabsley MJ, Miller KV (2015a) Epizootiology of cranial abscess disease in white-tailed deer (Odocoileus virginianus) of Georgia, USA. J Wildl Dis 51:609–618CrossRefPubMedGoogle Scholar
  7. Cohen BS, Belser EH, Keeler SP, Yabsley MJ, Miller KV (2015b) Isolation and genotypic characterization of Trueperella (Arcanobacterium) pyogenes recovered from active cranial abscess infections of male white-tailed deer (Odocoileus virginianus). J Zoo Wildl Med 46:62–67CrossRefPubMedGoogle Scholar
  8. Ding H, Lämmler C (1996) Purification and further characterization of a haemolysin of Actinomyces pyogenes. J Vet Med B Infect Dis Vet Public Health 43:179–188CrossRefGoogle Scholar
  9. Eisenberg T, Nagib S, Hijazin M, Alber J, Lämmler C, Hassan AA, Timke M, Kostrzewa M, Prenger-Berninghoff E, Schauerte N, Geiger C, Kaim U, Zschöck M (2012) Trueperella pyogenes as cause of a facial abscess in a grey slender loris (Loris lydekkerianus nordicus)—a case report. Berl Münch Tierärztl Wochenschr 125:407–410PubMedGoogle Scholar
  10. Ertaş HB, Kiliç A, Özbey G, Muz A (2005) Isolation of Arcanobacterium (Actinomyces) pyogenes from abscessed cattle kidney and identification by PCR. Turk J Vet Anim Sci 29:455–459Google Scholar
  11. Hassan AA, Ülbegi-Mohyla H, Kanbar T, Alber J, Lämmler C, Abdulmawjood A, Zschöck M, Weiss R (2009) Phenotypic and genotypic characterization of Arcanobacterium haemolyticum isolates from infections of horses. J Clin Microbiol 47:124–128CrossRefPubMedGoogle Scholar
  12. Hijazin M, Ulbegi-Mohyla H, Alber J, Lämmler C, Hassan AA, Abdulmawjood A, Prenger-Berninghoff E, Weiss R, Zschöck M (2011) Molecular identification and further characterization of Arcanobacterium pyogenes isolated from bovine mastitis and from various other origins. J Dairy Sci 94:1813–1819CrossRefPubMedGoogle Scholar
  13. Hijazin M, Hassan AA, Alber J, Lämmler C, Timke M, Kostrzewa M, Prenger-Berninghoff E, Zschöck M (2012a) Evaluation of matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS) for species identification of bacteria of genera Arcanobacterium and Trueperella. Vet Microbiol 157:243–245CrossRefPubMedGoogle Scholar
  14. Hijazin M, Prenger-Berninghoff E, Sammra O, Alber J, Lämmler C, Kämpfer P, Glaeser SP, Busse HJ, Hassan AA, Abdulmawjood A, Zschöck M (2012b) Arcanobacterium canis sp. nov., isolated from otitis externa of a dog, and emended description of the genus Arcanobacterium Collins et al. 1983 emend. Yassin et al. 2011. Int J Syst Evol Microbiol 62:2201–2205CrossRefPubMedGoogle Scholar
  15. Jost BH, Billington SJ (2005) Arcanobacterium pyogenes: molecular pathogenesis of an animal opportunist. A Van Leeuw J Microb 88:87–102CrossRefGoogle Scholar
  16. Lämmler C, Hartwigk H (1995) Actinomyces pyogenes und Arcanobacterium haemolyticum. In: Blobel H, Schließer T (eds) Handbuch der bakteriellen Infektionen bei Tieren, 2. edn. Gustav Fischer, Jena, pp 196–240 Band II/3Google Scholar
  17. Murray PR (2010) Matrix-assisted laser desorption ionization time of-flight mass spectrometry: usefulness for taxonomy and epidemiology. Clin Microbiol Infec 16:1626–1630CrossRefGoogle Scholar
  18. Plamondon M, Martinez G, Raynal L, Touchette M, Valiquette L (2007) A fatal case of Arcanobacterium pyogenes endocarditis in a man with no identified animal contact: case report and review of the literature. Eur J Clin Microbiol Infect Dis 26:663–666CrossRefPubMedGoogle Scholar
  19. Sammra O, Balbutskaya A, Nagib S, Alber J, Lämmler C, Abdulmawjood A, Timke M, Kostrzewa M, Prenger-Berninghoff E (2014) Properties of an Arcanobacterium haemolyticum strain isolated from a donkey. Berl Münch Tierärztl Wochenschr 127:10–14Google Scholar
  20. Santos TMA, Caixeta LS, Machado VS, Rauf AK, Gilbert RO, Bicalho RC (2010) Antimicrobial resistance and presence of virulence factor genes in Arcanobacterium pyogenes isolated from the uterus of postpartum dairy cows. Vet Microbiol 145:84–89CrossRefPubMedGoogle Scholar
  21. Seng P, Drancourt M, Gouriet F, La Scola B, Fournier PE, Rolain JM, Raoult D (2009) Ongoing revolution in bacteriology: routine identification of bacteria by matrix-assisted laser desorption ionization time-of-flight mass spectrometry. Clinic Inf Dis 49:543–551CrossRefGoogle Scholar
  22. Silva E, Gaivão M, Leitão S, Jost BH, Carneiro C, Vilela CL, Lopes da Costa L, Mateus L (2008) Genomic characterization of Arcanobacterium pyogenes isolates recovered from the uterus of dairy cows with normal puerperium or clinical metritis. Vet Microbiol 25:111–118CrossRefGoogle Scholar
  23. Ülbegi-Mohyla H, Hassan AA, Kanbar T, Alber J, Lämmler C, Prenger-Berninghoff E, Weiss R, Siebert U, Zschöck M (2009) Synergistic and antagonistic hemolytic activities of bacteria of genus Arcanobacterium and CAMP-like hemolysis of Arcanobacterium phocae and Arcanobacterium haemolyticum with Psychrobacter phenylpyruvicus. Res Vet Sci 87:186–188CrossRefPubMedGoogle Scholar
  24. Ülbegi-Mohyla H, Hijazin M, Alber J, Lämmler C, Hassan AA, Abdulmawjood A, Prenger-Berninghoff E, Weiss R, Siebert U, Zschöck M (2010a) Identification of Arcanobacterium pyogenes isolated by post mortem examinations of a bearded dragon and a gecko by phenotypic and genotypic properties. J Vet Sci 11:265–267CrossRefPubMedPubMedCentralGoogle Scholar
  25. Ülbegi-Mohyla H, Hassan AA, Alber J, Lämmler C, Prenger-Berninghoff E, Weiss R, Zschöck M (2010b) Identification of Arcanobacterium pluranimalium isolated from a dog by phenotypic properties and by PCR mediated characterization of various molecular targets. Vet Microbiol 142:458–460CrossRefPubMedGoogle Scholar
  26. Wickhorst J-P, Hassan AA, Sammra O, Huber-Schlenstedt R, Lämmler C, Prenger-Berninghoff E, Timke M, Abdulmawjood A (2016) Phenotypic and genotypic approach to characterize Arcanobacterium pluranimalium isolated from bovine milk samples. Folia Microbiol (Praha) 61:405–412CrossRefGoogle Scholar
  27. Yassin AF, Hupfer H, Siering C, Schumann P (2011) Comparative chemotaxonomic and phylogenetic studies on the genus Arcanobacterium Collins et al., 1982 emend Lehnen et al., 2006: proposal for Trueperella gen. nov. and emended description of the genus Arcanobacterium. Int J Syst Evol Microbiol 61:1265–1274CrossRefPubMedGoogle Scholar
  28. Zhao K, Tian Y, Yue B, Wang H, Zhang X (2013) Virulence determinants and biofilm production among Trueperella pyogenes recovered from abscesses of captive forest musk deer. Arch Microbiol 195:203–209CrossRefPubMedGoogle Scholar

Copyright information

© Institute of Microbiology, Academy of Sciences of the Czech Republic, v.v.i. 2017

Authors and Affiliations

  • Jörn-Peter Wickhorst
    • 1
  • Abdulwahed Ahmed Hassan
    • 2
  • Omar Hashim Sheet
    • 2
  • Tobias Eisenberg
    • 3
  • Osama Sammra
    • 1
  • Mazen Alssahen
    • 1
  • Christoph Lämmler
    • 1
  • Ellen Prenger-Berninghoff
    • 4
  • Michael Zschöck
    • 3
  • Markus Timke
    • 5
  • Amir Abdulmawjood
    • 6
  1. 1.Institut für Pharmakologie und ToxikologieJustus-Liebig-Universität GießenGiessenGermany
  2. 2.Department of Veterinary Public Health, College of Veterinary MedicineUniversity of MosulMosulIraq
  3. 3.Landesbetrieb Hessisches LandeslaborGiessenGermany
  4. 4.Institut für Hygiene und Infektionskrankheiten der TiereJustus-Liebig-Universität GießenGiessenGermany
  5. 5.Entwicklung BioanalyseBruker Daltonik GmbHBremenGermany
  6. 6.Institute of Food Quality and Food Safety, Research Center for Emerging Infections and Zoonoses (RIZ)University of Veterinary Medicine Hannover, FoundationHannoverGermany

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