Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-26T02:56:07.789Z Has data issue: false hasContentIssue false
  • English
  • Français

Multi-locus sequence typing confirms the clonality of Trichomonas gallinae isolates circulating in European finches

Published online by Cambridge University Press:  13 December 2013

PETRA GANAS ,
BARBARA JASKULSKA ,
BECKI LAWSON ,
MARKO ZADRAVEC ,
MICHAEL HESS  and
IVANA BILIC
PETRA GANAS
Affiliation:
Clinic for Avian, Reptile and Fish Medicine, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, Veterinärplatz 1, 1210 Vienna, Austria
BARBARA JASKULSKA
Affiliation:
Clinic for Avian, Reptile and Fish Medicine, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, Veterinärplatz 1, 1210 Vienna, Austria
BECKI LAWSON
Affiliation:
Institute of Zoology, Zoological Society of London, Regents Park, London NW1 4RY, UK
MARKO ZADRAVEC
Affiliation:
Veterinary Faculty, Institute for Poultry Health, University of Ljubljana, Gerbičeva 60, 1000 Ljubljana, Slovenia
MICHAEL HESS
Affiliation:
Clinic for Avian, Reptile and Fish Medicine, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, Veterinärplatz 1, 1210 Vienna, Austria
IVANA BILIC*
Affiliation:
Clinic for Avian, Reptile and Fish Medicine, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, Veterinärplatz 1, 1210 Vienna, Austria
*
* Corresponding author: Clinic for Avian, Reptile and Fish Medicine, University of Veterinary Medicine Vienna, Veterinärplatz 1, 1210 Vienna, Austria. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

In recent years, Trichomonas gallinae emerged as the causative agent of an infectious disease of passerine birds in Europe leading to epidemic mortality of especially greenfinches Chloris chloris and chaffinches Fringilla coelebs. After the appearance of finch trichomonosis in the UK and Fennoscandia, the disease spread to Central Europe. Finch trichomonosis first reached Austria and Slovenia in 2012. In the present study the genetic heterogeneity of T. gallinae isolates from incidents in Austria and Slovenia were investigated and compared with British isolates. For this purpose comparative sequence analyses of the four genomic loci ITS1-5.8S-ITS2, 18S rRNA, rpb1 and Fe-hydrogenase were performed. The results corroborate that one clonal T. gallinae strain caused the emerging infectious disease within passerine birds and that the disease is continuing to spread in Europe. The same clonal strain was also found in a columbid bird from Austria. Additionally, the present study demonstrates clearly the importance of multi-locus sequence typing for discrimination of circulating T. gallinae strains.

Keywords

Trichomonas gallinaefinch trichomonosisemerging infectious diseasepasserine birdsEuropean finchessequence analysisITS1-5.8S-ITS218S rRNAFe-hydrogenaserpb1
Type
Research Article
Information
Parasitology , Volume 141 , Issue 5 , April 2014 , pp. 652 - 661
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Amin, A., Bilic, I., Berger, E. and Hess, M. (2012 a). Trichomonas gallinae, in comparison to Tetratrichomonas gallinarum, induces distinctive cytopathogenic effects in tissue cultures. Veterinary Parasitology 186, 196–206. doi: 10.1016/j.vetpar.2011.11.037.CrossRefGoogle ScholarPubMed
Amin, A., Nobauer, K., Patzl, M., Berger, E., Hess, M. and Bilic, I. (2012 b). Cysteine peptidases, secreted by Trichomonas gallinae, are involved in the cytopathogenic effects on a permanent chicken liver cell culture. PLoS ONE 7, e37417. doi: 10.1371/journal.pone.0037417.CrossRefGoogle ScholarPubMed
Anderson, N. L., Grahn, R. A., Van Hoosear, K. and Bondurant, R. H. (2009). Studies of trichomonad protozoa in free ranging songbirds: prevalence of Trichomonas gallinae in house finches (Carpodacus mexicanus) and corvids and a novel trichomonad in mockingbirds (Mimus polyglottos). Veterinary Parasitology 161, 178–186. doi: 10.1016/j.vetpar.2009.01.23.Google Scholar
Archambault, J. and Friesen, J. D. (1993). Genetics of eukaryotic RNA polymerases I, II, and III. Microbiological Reviews 57, 703–724.Google Scholar
Bondurant, R. and Honigberg, B. M. (1994). Trichomonads of veterinary importance. In Parasitic Protozoa (ed. Kreier, J. P.), pp. 112–188. Academic Press, San Diego, CA.Google Scholar
Chi, J. F., Lawson, B., Durrant, C., Beckmann, K., John, S., Alrefaei, A. F., Kirkbride, K., Bell, D. J., Cunningham, A. A. and Tyler, K. M. (2013). The finch epidemic strain of Trichomonas gallinae is predominant in British non-passerines. Parasitology 140, 1234–1245.Google Scholar
Cramer, P., Bushnell, D. A., Fu, J., Gnatt, A. L., Maier-Davis, B., Thompson, N. E., Burgess, R. R., Edwards, A. M., David, P. R. and Kornberg, R. D. (2000). Architecture of RNA polymerase II and implications for the transcription mechanism. Science 288, 640–649.Google Scholar
Felleisen, R. S. (1997). Comparative sequence analysis of 5.8S rRNA genes and internal transcribed spacer (ITS) regions of trichomonadid protozoa. Parasitology 115, 111–119.Google Scholar
Forrester, D. J. and Foster, G. W. (2008). Trichomonosis. In Parasitic Diseases of Wild Birds (ed. Atkinson, C. T., Thomas, N. J. and Hunter, D. B.), pp. 120–153. Wiley-Blackwell, Ames, IA, USA.Google Scholar
Forzan, M. J., Vanderstichel, R., Melekhovets, Y. F. and McBurney, S. (2010). Trichomoniasis in finches from the Canadian Maritime provinces – an emerging disease. Canadian Veterinary Journal 51, 391–396.Google Scholar
Gerbod, D., Sanders, E., Moriya, S., Noel, C., Takasu, H., Fast, N. M., Delgado-Viscogliosi, P., Ohkuma, M., Kudo, T., Capron, M., Palmer, J. D., Keeling, P. J. and Viscogliosi, E. (2004). Molecular phylogenies of Parabasalia inferred from four protein genes and comparison with rRNA trees. Molecular Phylogenetics and Evolution 31, 572–580. doi: 10.1016/j.ympev.2003.09.013.Google Scholar
Gerhold, R. W., Yabsley, M. J., Smith, A. J., Ostergaard, E., Mannan, W., Cann, J. D. and Fischer, J. R. (2008). Molecular characterization of the Trichomonas gallinae morphologic complex in the United States. Journal of Parasitology 94, 1335–1341. doi: 10.1645/GE-1585.1.Google Scholar
Gourlay, P., Decors, A., Jouet, D., Treilles, D., Lemberger, K., Faure, E., Moinet, M., Chi, J., Tyler, K., Cunningham, A. and Lawson, B. (2011). Finch trichomonosis spreads to France. European Section of Wildlife Disease Association Bulletin 2, 9–10.Google Scholar
Grabensteiner, E., Bilic, I., Kolbe, T. and Hess, M. (2010). Molecular analysis of clonal trichomonad isolates indicate the existence of heterogenic species present in different birds and within the same host. Veterinary Parasitology 172, 53–64. doi: 10.1016/j.vetpar.2010.04.015.Google Scholar
Hess, M., Kolbe, T., Grabensteiner, E. and Prosl, H. (2006). Clonal cultures of Histomonas meleagridis, Tetratrichomonas gallinarum and a Blastocystis sp. established through micromanipulation. Parasitology 133, 547–554. doi: 10.1017/S0031182006000758.CrossRefGoogle Scholar
Keeling, P. J. (2004). Polymorphic insertions and deletions in parabasalian enolase genes. Journal of Molecular Evolution 58, 550–556. doi: 10.1007/s00239-003-2577-4.CrossRefGoogle ScholarPubMed
Kleina, P., Bettim-Bandinelli, J., Bonatto, S. L., Benchimol, M. and Bogo, M. R. (2004). Molecular phylogeny of Trichomonadidae family inferred from ITS-1, 5.8S rRNA and ITS-2 sequences. International Journal of Parasitology 34, 963–970. doi: 10.1016/j.ijpara.2004.04.004.CrossRefGoogle ScholarPubMed
Kocan, R. M. and Herman, C. M. (1971). Trichomoniasis. In Infectious and Parasitic Diseases of Wild Birds (ed. Davis, J. W., Anderson, R. C., Karstad, L. and Trainer, D. O.), pp. 282–290. Iowa State University Press, Ames, IA, USA.Google Scholar
Lawson, B., Cunningham, A., Chantrey, J., Hughes, L., Kirkwood, J., Pennycott, T. and Simpson, V. (2006). Epidemic finch mortality. Veterinary Record 159, 367. doi: 10.1136/vr.159.11.367-a.Google Scholar
Lawson, B., Cunningham, A. A., Chantrey, J., Hughes, L. A., John, S. K., Bunbury, N., Bell, D. J. and Tyler, K. M. (2011 a). A clonal strain of Trichomonas gallinae is the aetiologic agent of an emerging avian epidemic disease. Infection, Genetics and Evolution 11, 1638–1645. doi: 10.1016/j.meegid.2011.06.007.Google Scholar
Lawson, B., Robinson, R. A., Neimanis, A., Handeland, K., Isomursu, M., Agren, E. O., Hamnes, I. S., Tyler, K. M., Chantrey, J., Hughes, L. A., Pennycott, T. W., Simpson, V. R., John, S. K., Peck, K. M., Toms, M. P., Bennett, M., Kirkwood, J. K. and Cunningham, A. A. (2011 b). Evidence of spread of the emerging infectious disease, finch trichomonosis, by migrating birds. Ecohealth 8, 143–153. doi: 10.1007/s10393-011-0696-8.Google Scholar
Lawson, B., Robinson, R. A., Colvile, K. M., Peck, K. M., Chantrey, J., Pennycott, T. W., Simpson, V. R., Toms, M. P. and Cunningham, A. A. (2012). The emergence and spread of finch trichomonosis in the British Isles. Philosophical Transactions of the Royal Society London B: Biological Sciences 367, 2852–2863. doi: 10.1098/rstb.2012.0130.Google Scholar
Lehikoinen, A., Lehikoinen, E., Valkama, J., Väisänen, R. A. and Isomursu, M. (2013). Impacts of trichomonosis epidemics on Greenfinch Chloris chloris and Chaffinch Fringilla coelebs populations in Finland. IBIS The International Journal of Avian Science 155, 357–366.Google Scholar
Locke, L. N. and James, P. (1962). Trichomonad canker in the Inca Dove, Scardafella inca (Lesson). Journal of Parasitology 48, 497.Google Scholar
Malik, S. B., Brochu, C. D., Bilic, I., Yuan, J., Hess, M., Logsdon, J. M. Jr. and Carlton, J. M. (2011). Phylogeny of parasitic parabasalia and free-living relatives inferred from conventional markers vs. Rpb1, a single-copy gene. PLoS ONE 6, e20774. doi: 10.1371/journal.pone.0020774.Google Scholar
Neimanis, A. S., Handeland, K., Isomursu, M., Agren, E., Mattsson, R., Hamnes, I. S., Bergsjo, B. and Hirvela-Koski, V. (2010). First report of epizootic trichomoniasis in wild finches (family Fringillidae) in southern Fennoscandia. Avian Diseases 54, 136–141. doi: 10.1637/8952-060509-Case.1.Google Scholar
Norman, D. (2002). Chaffinch Fringilla coelebs . In The Migration Atlas: Movements of the Birds of Britain and Ireland (ed. Wenham, C. V., Toms, M. P., Marchant, J. H., Clark, J. A., Siriwardena, G. M. and Baille, S. R.), pp. 637–640. T. & A.D. Poyser, London, UK.Google Scholar
NWHC (2002). 1983–2006. Epizootic Files. United States Geological Survey, National Wildlife Health Center, Madison, WI, USA.Google Scholar
Pennycott, T., Lawson, B., Cunningham, A., Simpson, V. and Chantrey, J. (2005). Necrotic ingluvitis in wild finches. Veterinary Record 157, 360. doi: 10.1136/vr.157.12.360.Google Scholar
Peters, M., Kilwinski, J., Reckling, D. and Henning, K. (2009). Gehäufte Todesfälle von wild lebenden Grünfinken an Futterstellen infolge Trichomonas-gallinae-Infektionen – ein aktuelles Probel in Norddeutschland. Kleintierpraxis 54, 433–438.Google Scholar
Robinson, R. A., Lawson, B., Toms, M. P., Peck, K. M., Kirkwood, J. K., Chantrey, J., Clatworthy, I. R., Evans, A. D., Hughes, L. A., Hutchinson, O. C., John, S. K., Pennycott, T. W., Perkins, M. W., Rowley, P. S., Simpson, V. R., Tyler, K. M. and Cunningham, A. A. (2010). Emerging infectious disease leads to rapid population declines of common British birds. PLoS ONE 5, e12215. doi: 10.1371/journal.pone.0012215.CrossRefGoogle ScholarPubMed
Rogers, M. B., Watkins, R. F., Harper, J. T., Durnford, D. G., Gray, M. W. and Keeling, P. J. (2007). A complex and punctate distribution of three eukaryotic genes derived by lateral gene transfer. BMC Evolutionary Biology 7, 89. doi: 10.1186/1471-2148-7-89.Google Scholar
Sansano-Maestre, J., Garijo-Toledo, M. M. and Gomez-Munoz, M. T. (2009). Prevalence and genotyping of Trichomonas gallinae in pigeons and birds of prey. Avian Pathology 38, 201–207. doi: 10.1080/03079450902912135.Google Scholar
Stabler, R. M. (1954). Trichomonas gallinae: a review. Experimental Parasitology 3, 368–402.Google Scholar
Stechmann, A., Baumgartner, M., Silberman, J. D. and Roger, A. J. (2006). The glycolytic pathway of Trimastix pyriformis is an evolutionary mosaic. BMC Evolutionary Biology 6, 101. doi: 10.1186/1471-2148-6-101.Google Scholar
Vignais, P. M. and Billoud, B. (2007). Occurrence, classification, and biological function of hydrogenases: an overview. Chemical Reviews 107, 4206–4272. doi: 10.1021/cr050196r.Google Scholar
Viscogliosi, E. and Müller, M. (1998). Phylogenetic relationships of the glycolytic enzyme, glyceraldehyde-3-phosphate dehydrogenase, from parabasalid flagellates. Journal of Molecular Evolution 47, 190–199.Google Scholar
Wu, G., Fiser, A., ter, K. B., Sali, A. and Muller, M. (1999). Convergent evolution of Trichomonas vaginalis lactate dehydrogenase from malate dehydrogenase. Proceedings of the National Academy of Sciences USA 96, 6285–6290. doi: 10.1073/pnas.96.11.6285.CrossRefGoogle ScholarPubMed
Zadravec, M., Marhold, C., Slavec, B., Rojs, O. Z. and Racnik, J. (2012). Trichomonosis in finches in Slovenia. Veterinary Record 171, 253–254. doi: 10.1136/vr.e5973.Google Scholar