Folia Parasitologica 68:019 (2021) | DOI: 10.14411/fp.2021.019

How monoxenous trypanosomatids revealed hidden feeding habits of their tsetse fly hosts

Jan Votýpka ORCID...1,2,*, Klára J. Petrželková2,3,4, Jana Brzoňová ORCID...1, Milan Jirků2, David Modrý ORCID...2,5,6, Julius Lukeš ORCID...2,7,*
1 Department of Parasitology, Faculty of Science, Charles University, Prague, Czech Republic;
2 Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice (Budweis), Czech Republic;
3 Institute of Vertebrate Biology, Czech Academy of Sciences, Studenec, Czech Republic;
4 Liberec Zoo, Liberec, Czech Republic;
5 Department of Botany and Zoology, Faculty of Science, Masaryk University, Brno, Czech Republic;
6 Department of Veterinary Sciences, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences, Prague, Czech Republic;
7 Faculty of Sciences, University of South Bohemia, České Budějovice (Budweis), Czech Republic
* corresponding author

Tsetse flies are well-known vectors of trypanosomes pathogenic for humans and livestock. For these strictly blood-feeding viviparous flies, the host blood should be the only source of nutrients and liquids, as well as any exogenous microorganisms colonising their intestine. Here we describe the unexpected finding of several monoxenous trypanosomatids in their gut. In a total of 564 individually examined Glossina (Austenia) tabaniformis (Westwood) (436 specimens) and Glossina (Nemorhina) fuscipes fuscipes (Newstead) (128 specimens) captured in the Dzanga-Sangha Protected Areas, Central African Republic, 24 (4.3%) individuals were infected with monoxenous trypanosomatids belonging to the genera Crithidia Léger, 1902; Kentomonas Votýpka, Yurchenko, Kostygov et Lukeš, 2014; Novymonas Kostygov et Yurchenko, 2020; Obscuromonas Votýpka et Lukeš, 2021; and Wallacemonas Kostygov et Yurchenko, 2014. Moreover, additional 20 (3.5%) inspected tsetse flies harboured free-living bodonids affiliated with the genera Dimastigella Sandon, 1928; Neobodo Vickerman, 2004; Parabodo Skuja, 1939; and Rhynchomonas Klebs, 1892. In the context of the recently described feeding behaviour of these dipterans, we propose that they become infected while taking sugar meals and water, providing indirect evidence that blood is not their only source of food and liquids.

Keywords: Glossina, blood-feeding, adenotrophic viviparity, bodonids, Trypanosoma, infection.

Received: March 1, 2021; Revised: March 30, 2021; Accepted: April 22, 2021; Published online: July 19, 2021  Show citation

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Votýpka, J., Petrželková, K.J., Brzoňová, J., Jirků, M., Modrý, D., & Lukeš, J. (2021). How monoxenous trypanosomatids revealed hidden feeding habits of their tsetse fly hosts. Folia Parasitologica68, Article 2021.019. https://doi.org/10.14411/fp.2021.019
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References

  1. Buxton P.A. 1955: The Natural History of Tsetse Flies: An Account of the Biology of the Genus Glossina (Diptera). H. K. Lewis & Co., London, 739 pp.
  2. Dario M.A., Moratelli R., Schwabl P., Jansen A.M., Llewellyn M.S. 2017: Small subunit ribosomal metabarcoding reveals extraordinary trypanosomatid diversity in Brazilian bats. PLoS Negl. Trop. Dis. 11: e0005790. Go to original source... Go to PubMed...
  3. D'Costa M.A., Rice M.J., Latif A. 1973: Glycogen in the proventriculus of the tsetse fly. J. Insect Physiol. 19: 427-433. Go to original source... Go to PubMed...
  4. Dedet J.P., Pratlong F. 2000: Leishmania, Trypanosoma and monoxenous trypanosomatids as emerging opportunistic agents. J. Eukaryot. Microbiol. 47: 37-39. Go to original source... Go to PubMed...
  5. Doudoumis V., Blow F., Saridaki A., Augustinos A., Dyer N.A., Goodhead I., Solano P., Rayaisse J.-B., Takac P., Mekonnen S., Parker A.G., Abd-Alla A.M.M., Darby A., Bourtzis K., Tsiamis G. 2017: Challenging the Wigglesworthia, Sodalis, Wolbachia symbiosis dogma in tsetse flies: Spiroplasma is present in both laboratory and natural populations. Sci. Rep. 7: 4699. Go to original source... Go to PubMed...
  6. Flegontova O., Flegontov P., Londoño P.A.C., Walczowski W., Šantić D., Edgcomb V.P., Lukeš J., Horák A. 2020: Environmental determinants of the distribution of planktonic diplonemids and kinetoplastids in the oceans. Env. Microbiol. 22: 4014-4031. Go to original source... Go to PubMed...
  7. Frolov A.O., Kostygov A.Y., Yurchenko V. 2021: Development of monoxenous trypanosomatids and phytomonads in insects. Trends Parasitol. 37: 538-551. Go to original source... Go to PubMed...
  8. Gaithuma A., Yamagishi J., Hayashida K., Kawai N., Namangala B., Sugimoto Ch. 2020: Blood meal sources and bacterial microbiome diversity in wildcaught tsetse flies. Sci. Rep. 10: 5005. Go to original source... Go to PubMed...
  9. Ganyukova A.I., Malysheva M.N., Smirnov P.A., Frolov A.O. 2019: Crithidia dobrovolskii sp. n. (Kinetoplastida: Trypanosomatidae) from parasitoid fly Lypha dubia (Diptera: Tachinidae): morphology and phylogenetic position. Protistology 13: 206-214. Go to original source...
  10. Gibson W. 2017: Kinetoplastea. In: J.M. Archibald, A.G.B. Simpson, C.H. Slamovits (Eds.), Handbook of the Protists. Springer, Cham, pp. 1089-1138. Go to original source...
  11. Gómez-Moracho T., Buendía-Abad M., Benito M., García-Palencia P., Barrios L., Bartolomé C., Maside X., Meana A., Jiménez-Antón M.D., Olías-Molero A.I., Alunda J.M., Martín-Hernández R., Higes M. 2020: Experimental evidence of harmful effects of Crithidia mellificae and Lotmaria passim on honey bees. Int. J. Parasitol. 50: 1117-1124. Go to original source... Go to PubMed...
  12. Haines L.R., Vale G.A., Barreaux A.M.G., Ellstrand N.C., Hargrove J.W., English S. 2020: Big baby, little mother: tsetse flies are exceptions to the juvenile small size principle. BioEssays 42: 2000049. Go to original source... Go to PubMed...
  13. Hamilton P.T., Votýpka J., Dostálová A., Yurchenko V., Bird N.H., Lukeš J., Lemaitre B., Perlman S.J. 2015: Infection dynamics and immune response in a newly described Drosophila-trypanosomatid association. mBio 6: e01356-15. Go to original source... Go to PubMed...
  14. Kostygov A.Y., Karnkowska A., Votýpka J., Tashyreva D., Maciszewski K., Yurchenko V., Lukeš J. 2021: Euglenozoa: taxonomy, diversity and ecology, symbioses and viruses. Open Biol. 11: 200407. Go to original source... Go to PubMed...
  15. Kostygov A., Dobáková E., Grybchuk-Ieremenko A., Váhala D., Maslov D.A., Votýpka J., Lukeš J., Yurchenko V. 2016: Novel trypanosomatid-bacterium association: evolution of endosymbiosis in action. mBio 7: e01985-15. Go to original source... Go to PubMed...
  16. Leak S.G.A. 1998: Tsetse Biology and Ecology: Their Role in the Epidemiology and Control of Trypanosomosis. CABI, Wallingford, 568 pp. Go to original source...
  17. Lipa J.J. 1963: Infection caused by Protozoa other than Sporozoa. In: A.E. Steinhaus (Ed.), Insect Pathology. An Advanced Treatise. Academic Press, New York, pp. 335-358. Go to original source...
  18. Lukeš J., Tesařová M., Yurchenko V., Votýpka J. 2021: Characterization of a new cosmopolitan genus of trypanosomatid parasites, Obscuromonas gen. nov. (Blastocrithidiinae subfam. nov.). Eur. J. Protistol. 79: 125778. Go to original source... Go to PubMed...
  19. Lukeš J., Butenko A., Hashimi H., Maslov D.A., Votýpka J., Yurchenko V. 2018: Trypanosomatids are much more than just trypanosomes: clues from the expanded family tree. Trends Parasitol. 34: 466-480. Go to original source... Go to PubMed...
  20. Lukeš J., Skalický T., Týč J., Votýpka J., Yurchenko V. 2014: Evolution of parasitism in kinetoplastid flagellates. Mol. Biochem. Parasitol. 195: 115-122. Go to original source... Go to PubMed...
  21. Maslov D.A., Votýpka J., Yurchenko V., Lukeš J. 2013: Diversity and phylogeny of insect trypanosomatids: all that is hidden shall be revealed. Trends Parasitol. 29: 43-52. Go to original source... Go to PubMed...
  22. Ngoune J.M.T, Reveillaud J., Sempere G., Njiokou F., Melachio T.T., Abate L., Tchiofo M.T., Geiger A. 2019: The composition and abundance of bacterial communities residing in the gut of Glossina palpalis palpalis captured in two sites of southern Cameroon. Parasit. Vectors 12: 151. Go to original source... Go to PubMed...
  23. Podlipaev S.A. 1990: [Catalogue of World Fauna of Trypanosomatidae (Protozoa).] Zoologicheskii Institut AN SSSR, Leningrad, 177 pp. (In Russian.)
  24. Schaub G.A. 1994: Pathogenicity of trypanosomatids on insects. Parasitol. Today 10: 463-468. Go to original source... Go to PubMed...
  25. Schwarz R.S., Bauchan G.R., Murphy C.A., Ravoet J., De Graaf D.C., Evans J.D., De Graaf D.C., Evans J.D. 2015: Characterization of two species of Trypanosomatidae from the honey bee Apis mellifera: Crithidia mellificae Langridge and McGhee, 1967 and Lotmaria passim n. gen., n. sp. J. Eukaryot. Microbiol. 62: 567-583. Go to original source... Go to PubMed...
  26. Scoones I. 2014: The Politics of Trypanosomiasis Control in Africa. STEPS Centre Working Paper 57, STEPS Centre, Brighton, 37 pp.
  27. Solano P., Salou E., Rayaisse J.-B., Ravel S., Gimonneau G., Traore I., Bouyer J. 2015: Do tsetse fies only feed on blood? Infect. Genet. Evol. 36: 184-189. Go to original source... Go to PubMed...
  28. Steverding D. 2008: The history of African trypanosomiasis. Parasit. Vectors 1: 3. Go to original source... Go to PubMed...
  29. Strobl V., Yañez O., Straub L., Albrecht M., Neumann P. 2019: Trypanosomatid parasites infecting managed honeybees and wild solitary bees. Int. J. Parasitol. 49: 605-613. Go to original source... Go to PubMed...
  30. Stuhlmann F. 1907: Beitrage zur Kenntnis der Tsetsefliege (Glossina fusca und Gl. tachinoides). Springer, Berlin-Heidelberg, 91 pp. Go to original source...
  31. Szőke K., Sándor A.D., Boldogh S.A., Görföl T., Votýpka J., Takács N., Estók P., Kováts D., Corduneanu A., Molnár V., Kontschánand J., Hornok S. 2017: DNA of free-living bodonids (Euglenozoa: Kinetoplastea) in bat ectoparasites: potential relevance to the evolution of parasitic trypanosomatids. Acta Vet. Hung. 65: 531-540. Go to original source... Go to PubMed...
  32. Teixeira M.M.G., Borghesan T.C., Ferreira R.C., Santos M.A., Takata C.S., Campaner M., Nunes V.L., Milder R.V., de Souza W., Camargo E.P. 2011: Phylogenetic validation of the genera Angomonas and Strigomonas of trypanosomatids harboring bacterial endosymbionts with the description of new species of trypanosomatids and of proteobacterial symbionts. Protist 162: 503-524. Go to original source... Go to PubMed...
  33. Votýpka J., Brzoňová J., Ježek J., Modrý D. 2019: Horse flies (Diptera: Tabanidae) of three West African countries: a faunistic update, barcoding analysis and trypanosome occurrence. Acta Trop. 197: 105069. Go to original source... Go to PubMed...
  34. Votýpka J., Kment P., Yurchenko V., Lukeš J. 2020: Endangered monoxenous trypanosomatid parasites: a lesson from island biogeography. Biodivers. Conserv. 29: 3635-3667. Go to original source...
  35. Votýpka J., Klepetková H., Jirků M., Kment P., Lukeš J. 2012: Phylogenetic relationships of trypanosomatids parasitizing true bugs (Insecta: Heteroptera) in sub-Saharan Africa. Int. J. Parasitol. 42: 489-500. Go to original source... Go to PubMed...
  36. Votýpka J., Kostygov A. Y., Kraeva N., Grybchuk-Ieremenko A., Tesařová M., Grybchuk D., Lukeš J., Yurchenko V. 2014: Kentomonas gen. g., a new genus of endosymbiont-containing trypanosomatids of Strigomonadinae subfam. n. Protist 165: 825-838. Go to original source... Go to PubMed...
  37. Votýpka J., Rádrová J., Skalický T., Jirků M., Jirsová D., Mihalca A.D., D'Amico G., Petrželková K.J., Modrý D., Lukeš J. 2015: A tsetse and tabanid fly survey of African great apes habitats reveals the presence of a novel trypanosome lineage but the absence of Trypanosoma brucei. Int. J. Parasitol. 45: 741-748. Go to original source... Go to PubMed...
  38. Vreysen M.J.B., Seck M.T., Sall B., Bouyer J. 2013: Tsetse flies: their biology and control using area-wide integrated pest management approaches. J. Invertebr. Pathol. 112: S15-S25. Go to original source... Go to PubMed...
  39. Wallace F.G. 1966: The trypanosomatid parasites of insects and arachnids. Exp. Parasitol. 18: 124-193. Go to original source... Go to PubMed...
  40. Wang J., Weiss B.L., Aksoy S. 2013: Tsetse fly microbiota: form and function. Front. Cell Infect. Microbiol. 3: 69. Go to original source... Go to PubMed...
  41. Westenberger S.J., Sturm N.R., Yanega D., Podlipaev S.A., Zeledon R., Campbell D.A., Maslov D.A. 2004: Trypanosomatid biodiversity in Costa Rica: genotyping of parasites from Heteroptera using the spliced leader RNA gene. Parasitology 129: 537-547. Go to original source... Go to PubMed...
  42. WHO 2012. Report of a WHO Meeting on Elimination of African Trypanosomiasis (Trypanosoma brucei gambiense). WHO, Geneva, 80 pp.
  43. Yurchenko V., Votýpka J., Tesařová M., Klepetková H., Kraeva N., Jirků M., Lukeš J. 2014: Ultrastructure and molecular phylogeny of four new species of monoxenous trypanosomatids from flies (Diptera: Brachycera) with redefinition of the genus Wallaceina. Folia Parasitol. 61: 97-112. Go to original source...