Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-20T07:33:21.376Z Has data issue: false hasContentIssue false

Trypanosomatids are common and diverse parasites of Drosophila

Published online by Cambridge University Press:  18 April 2011

L. WILFERT*
Affiliation:
Department of Genetics, University of Cambridge, Cambridge CB2 3EH, UK
B. LONGDON
Affiliation:
Institute of Evolutionary Biology and Centre for Immunity, Infection and Evolution, University of Edinburgh, Ashworth Laboratories, Kings Buildings, West Mains Road, Edinburgh EH9 3JT, UK
A. G. A. FERREIRA
Affiliation:
Department of Genetics, University of Cambridge, Cambridge CB2 3EH, UK
F. BAYER
Affiliation:
Department of Genetics, University of Cambridge, Cambridge CB2 3EH, UK
F. M. JIGGINS
Affiliation:
Department of Genetics, University of Cambridge, Cambridge CB2 3EH, UK
*
*Corresponding author: Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3JT, UK. Tel: +44 131650 8683. Fax: +44 131650 6564. E-mail: [email protected]

Summary

Drosophila melanogaster is an important model system of immunity and parasite resistance, yet most studies use parasites that do not naturally infect this organism. We have studied trypanosomatids in natural populations to assess the prevalence and diversity of these gut parasites. We collected several species of Drosophila from Europe and surveyed them for trypanosomatids using conserved primers for two genes. We have used the conserved GAPDH sequence to construct a phylogenetic tree and the highly variable spliced leader RNA to assay genetic diversity. All 5 of the species that we examined were infected, and the average prevalence ranged from 1 to 6%. There are several different groups of trypanosomatids, related to other monoxenous Trypanosomatidae. These may represent new trypanosomatid species and were found in different species of European Drosophila from different geographical locations. The detection of a little studied natural pathogen in D. melanogaster and related species provides new opportunities for research into both the Drosophila immune response and the evolution of hosts and parasites.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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

Boulanger, N., Ehret-Sabatier, L., Brun, R., Zachary, D., Bulet, P. and Imler, J. L. (2001). Immune response of Drosophila melanogaster to infection with the flagellate parasite Crithidia spp. Insect Biochemistry and Molecular Biology 31, 129137.CrossRefGoogle ScholarPubMed
Brun, P. and Plus, N. (1980). The viruses of Drosophila. In The Genetics and Biology of Drosophila (ed. by Ashburner, M. and Wright, T. R. F.), pp. 625702. Academic Press, London, UK.Google Scholar
Chatton, E. and Alilaire, E. (1908). Coexistence d'un Leptomonas (Herpetomonas) et d'un Trypanosoma chez un muscide non vulnérant, Drosophila confusa Staeger. Comptes rendus des Seances de la Societe de Biologie, Paris 64, 10041006.Google Scholar
Chatton, E. and Leger, A. (1911). Eutrypanosomes, Leptomonas et Leptotrypanosomes chez Drosophila confusa Staeger (Muscide). Comptes rendus des Seances de la Societe de Biologie, Paris 70, 3436.Google Scholar
Corby-Harris, V., Pontaroli, A. C., Shimkets, L. J., Bennetzen, J. L., Habel, K. E. and Promislow, D. E. L. (2007). Geographical distribution and diversity of bacteria associated with natural populations of Drosophila melanogaster. Applied and Environmental Microbiology 73, 34703479. doi: 10.1128/aem.02120-06.CrossRefGoogle ScholarPubMed
Douady, C. J., Delsuc, F., Boucher, Y., Doolittle, W. F. and Douzery, E. J. P. (2003). Comparison of Bayesian and maximum likelihood bootstrap measures of phylogenetic reliability. Molecular Biology and Evolution 20, 248254. doi: 10.1093/molbev/msg042.CrossRefGoogle ScholarPubMed
Ebbert, M. A., Burkholder, J. J. and Marlowe, J. L. (2001). Trypanosomatid prevalence and host habitat choice in woodland Drosophila. Journal of Invertebrate Pathology 77, 2732. doi:10.1006/jipa.2000.4989.CrossRefGoogle ScholarPubMed
Ebbert, M. A., Marlowe, J. L. and Burkholder, J. J. (2003). Protozoan and intracellular fungal gut endosymbionts in Drosophila: prevalence and fitness effects of single and dual infections. Journal of Invertebrate Pathology 83, 3745. doi: 10.1016/s0022-2011(03)00033-8.CrossRefGoogle ScholarPubMed
Felsenstein, J. (2005). PHYLIP (Phylogeny Inference Package) Version 3.69. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle.Google Scholar
Guindon, S. and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696704. doi:10.1080/10635150390235520.CrossRefGoogle ScholarPubMed
Hoffmann, J. A. (2003). The immune response of Drosophila. Nature 426, 3338. doi: 10.1038/nature02021.CrossRefGoogle ScholarPubMed
Huelsenbeck, J. P. and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754755. doi: 10.1093/bioinformatics/17.8.754.CrossRefGoogle ScholarPubMed
Juneja, P. and Lazzaro, B. P. (2009). Providencia sneebia sp. nov. and Providencia burhodogranariea sp. nov., isolated from wild Drosophila melanogaster. International Journal of Systematic and Evolutionary Microbiology 59, 11081111. doi:10.1099/ijs.0.000117-0.CrossRefGoogle ScholarPubMed
Lewontin, R. C. and Felsenstein, J. (1965). The robustness of homogeneity tests in 2 X n tables. Biometrics 21, 1933.CrossRefGoogle Scholar
Longdon, B., Obbard, D. J. and Jiggins, F. M. (2010). Sigma viruses from three species of Drosophila form a major new clade in the rhabdovirus phylogeny. Proceedings of the Royal Society of London, B 277, 3544. doi:10.1098/rspb.2009.1472.Google Scholar
Maslov, D. A., Westenberger, S. J., Xu, X., Campbell, D. A. and Sturm, N. R. (2007). Discovery and barcoding by analysis of spliced leader RNA gene sequences of new isolates of Trypanosomatidae from Heteroptera in Costa Rica and Ecuador. Journal of Eukaryotic Microbiology 54, 5765. doi:10.1111/j.1550-7408.2006.00150.x.CrossRefGoogle ScholarPubMed
Maslov, D. A., Yurchenko, V. Y., Jirku, M. and Lukes, J. (2010). Two new species of trypanosomatid parasites isolated from Heteroptera in Costa Rica. Journal of Eukaryotic Microbiology 57, 177188. doi: 10.1111/j.1550-7408.2009.00464.x.CrossRefGoogle ScholarPubMed
McGhee, R. B. and Cosgrove, W. B. (1980). Biology and physiology of the lower Trypanosomatidae. Microbiological Reviews 44, 140173.CrossRefGoogle ScholarPubMed
McGhee, R. B., Hanson, W. L. and Schmittner, S. M. (1969). Isolation, cloning and determination of biologic characteristics of five new species of Crithidia. Journal of Eukaryotic Microbiology 16, 514520. doi: 10.1111/j.1550-7408.1969.tb02310.x.Google ScholarPubMed
Murthy, V. K., Dibbern, K. M. and Campbell, D. A. (1992). PCR amplification of mini-exon genes differentiates Trypanosoma cruzi from Trypanosoma rangeli. Molecular and Cellular Probes 6, 237243. doi:10.1016/0890-8508(92)90022-P.CrossRefGoogle ScholarPubMed
Ogden, T. H. and Rosenberg, M. S. (2006). Multiple sequence alignment accuracy and phylogenetic inference. Systematic Biology 55, 314328. doi: 10.1080/10635150500541730.CrossRefGoogle ScholarPubMed
Podlipaev, S. (2001). The more insect trypanosomatids under study-the more diverse Trypanosomatidae appears. International Journal for Parasitology 31, 647651. doi: 10.1016/S0020-7519(01)00139-4.CrossRefGoogle ScholarPubMed
Podlipaev, S. A., Sturm, N. R., Fiala, I., Fernanades, O., Westenberger, S. J., Dollet, M., Campbell, D. A. and Lukes, J. (2004). Diversity of insect trypanosomatids assessed from the spliced leader RNA and 5S rRNA genes and intergenic regions. Journal of Eukaryotic Microbiology 51, 283290.CrossRefGoogle ScholarPubMed
Posada, D. (2008). jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution 25, 12531256. doi: 10.1093/molbev/msn083.CrossRefGoogle ScholarPubMed
Rowton, E. D. and McGhee, R. B. (1983). Transmission of Herpetomonas in Laboratory Populations of Drosophila melanogaster. Journal of Eurkaryotic Microbiology 30, 669671. doi: 10.1111/j.1550-7408.1983.tb05341.x.Google Scholar
Swofford, D. L. (2003). PAUP*. Phylogenetic Analysis using Parsimony (*and other Methods) Sinauer Associates, Sunderland, MA, USA.Google Scholar
Thomas, S., Westenberger, S. J., Campbell, D. A. and Sturm, N. R. (2005). Intragenomic spliced leader RNA array analysis of kinetoplastids reveals unexpected transcribed region diversity in Trypanosoma cruzi. Gene 352, 100108. doi: 10.1016/j.gene.2005.04.002.CrossRefGoogle ScholarPubMed
Westenberger, S. J., Sturm, N. R., Yanega, D., Podlipaev, S. A., Zeledon, N. R., Campbell, D. A. and Maslov, D. A. (2004). Trypanosomatid biodiversity in Costa Rica: genotyping of parasites from Heteroptera using the spliced leader RNA gene. Parasitology 129, 537547. doi: 10.1017/S003118200400592X.CrossRefGoogle ScholarPubMed
Votypka, J., Maslov, D. A., Yurchenko, V., Jirku, M., Kment, P., Lun, Z. R. and Lukes, J. (2010). Probing into the diversity of trypanosomatid flagellates parasitizing insect hosts in South-West China reveals both endemism and global dispersal. Molecular Phylogenetics and Evolution 54, 243253. doi: 10.1016/j.ympev.2009.10.014.CrossRefGoogle ScholarPubMed
Yurchenko, V. Y., Lukes, J., Jirku, M. and Maslov, D. A. (2009). Selective recovery of the cultivation-prone components from mixed trypanosomatid infections: a case of several novel species isolated from neotropical Heteroptera. International Journal of Systematic and Evolutionary Microbiology 59, 893909. doi: 10.1099/ijs.0.001149-0.CrossRefGoogle ScholarPubMed
Yurchenko, V., Lukes, J., Xu, X. and Maslov, D. A. (2006). An integrated morphological and molecular approach to a new species description in the trypanosomatidae: The case of Leptomonas podlipaevi n. Sp., a parasite of Boisea rubrolineata (Hemiptera : Rhopalidae). Journal of Eukaryotic Microbiology 53, 103111. doi: 103-111. 10.1111/j.1550-7408.2005.00078.x.CrossRefGoogle Scholar
Supplementary material: File

Wilfert Supplementary Figure

Wilfert Supplementary Figure

Download Wilfert Supplementary Figure(File)
File 1.2 MB