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Trypanosomatids are common and diverse parasites of Drosophila

  • L. WILFERT (a1), B. LONGDON (a2), A. G. A. FERREIRA (a1), F. BAYER (a1) and F. M. JIGGINS (a1)...
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.

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Corresponding author
*Corresponding author: Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3JT, UK. Tel: +44 131650 8683. Fax: +44 131650 6564. E-mail: lena.wilfert@ed.ac.uk
References
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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.
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.
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.
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.
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.
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.
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.
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.
Felsenstein, J. (2005). PHYLIP (Phylogeny Inference Package) Version 3.69. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle.
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.
Hoffmann, J. A. (2003). The immune response of Drosophila. Nature 426, 3338. doi: 10.1038/nature02021.
Huelsenbeck, J. P. and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754755. doi: 10.1093/bioinformatics/17.8.754.
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.
Lewontin, R. C. and Felsenstein, J. (1965). The robustness of homogeneity tests in 2 X n tables. Biometrics 21, 1933.
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.
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.
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.
McGhee, R. B. and Cosgrove, W. B. (1980). Biology and physiology of the lower Trypanosomatidae. Microbiological Reviews 44, 140173.
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.
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.
Ogden, T. H. and Rosenberg, M. S. (2006). Multiple sequence alignment accuracy and phylogenetic inference. Systematic Biology 55, 314328. doi: 10.1080/10635150500541730.
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.
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.
Posada, D. (2008). jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution 25, 12531256. doi: 10.1093/molbev/msn083.
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.
Swofford, D. L. (2003). PAUP*. Phylogenetic Analysis using Parsimony (*and other Methods) Sinauer Associates, Sunderland, MA, USA.
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.
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.
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.
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.
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.
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Parasitology
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