Obligate development of Blastocrithidia papi (Trypanosomatidae) in the Malpighian tubules of Pyrrhocoris apterus (Hemiptera) and coordination of host-parasite life cycles

. 2018 ; 13 (9) : e0204467. [epub] 20180927

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid30261003

Blastocrithidia papi is a unique trypanosomatid in that its life cycle is synchronized with that of its host, and includes an obligate stage of development in Malpighian tubules (MTs). This occurs in firebugs, which exited the winter diapause. In the short period, preceding the mating of overwintered insects, the flagellates penetrate MTs of the host, multiply attached to the epithelial surface with their flagella, and start forming cyst-like amastigotes (CLAs) in large agglomerates. By the moment of oviposition, a large number of CLAs are already available in the rectum. They are discharged on the eggs' surface with feces, used for transmission of bugs' symbiotic bacteria, which are compulsorily engulfed by the newly hatched nymphs along with the CLAs. The obligate development of B. papi in MTs is definitely linked to the life cycle synchronization. The absence of peristalsis allow the trypanosomatids to accumulate and form dense CLA-forming subpopulations, whereas the lack of peritrophic structures facilitates the extensive discharge of CLAs directly into the hindgut lumen. The massive release of CLAs associated with oviposition is indispensable for maximization of the infection efficiency at the most favorable time point.

Erratum v

PubMed

Zobrazit více v PubMed

Wallace FG. The trypanosomatid parasites of insects and arachnids. Exp Parasitol. 1966;18(1): 124–93. PubMed

Podlipaev SA. [Catalogue of world fauna of Trypanosomatidae (Protozoa)]. Krylov MV, editor. Leningrad: Zoologicheskii Institut AN SSSR; 1990. 178 pp. (in Russian).

Maslov DA, Opperdoes FR, Kostygov AY, Hashimi H, Lukeš J, Yurchenko V. Recent advances in trypanosomatid research: genome organization, expression, metabolism, taxonomy and evolution. Parasitology. 2018;(in press). 10.1017/S0031182018000951 PubMed DOI

Maslov DA, Votýpka J, Yurchenko V, Lukeš J. Diversity and phylogeny of insect trypanosomatids: all that is hidden shall be revealed. Trends Parasitol. 2013;29(1): 43–52. 10.1016/j.pt.2012.11.001 PubMed DOI

Lukeš J, Butenko A, Hashimi H, Maslov DA, Votýpka J, Yurchenko V. Trypanosomatids are much more than just trypanosomes: clues from the expanded family tree. Trends Parasitol. 2018;34(6): 466–80. 10.1016/j.pt.2018.03.002 PubMed DOI

Merzlyak E, Yurchenko V, Kolesnikov AA, Alexandrov K, Podlipaev SA, Maslov DA. Diversity and phylogeny of insect trypanosomatids based on small subunit rRNA genes: polyphyly of Leptomonas and Blastocrithidia. J Eukaryot Microbiol. 2001;48(2): 161–9. PubMed

Hollar L, Lukeš J, Maslov DA. Monophyly of endosymbiont containing trypanosomatids: phylogeny versus taxonomy. J Eukaryot Microbiol. 1998;45(3): 293–7. PubMed

Kostygov AY, Grybchuk-Ieremenko A, Malysheva MN, Frolov AO, Yurchenko V. Molecular revision of the genus Wallaceina. Protist. 2014;165(5): 594–604. 10.1016/j.protis.2014.07.001 PubMed DOI

Votýpka J, d'Avila-Levy CM, Grellier P, Maslov DA, Lukeš J, Yurchenko V. New Approaches to Systematics of Trypanosomatidae: Criteria for Taxonomic (Re)description. Trends Parasitol. 2015;31(10): 460–9. 10.1016/j.pt.2015.06.015 PubMed DOI

Kostygov AY, Frolov AO. [Leptomonas jaculum (Leger, 1902) Woodcock 1914: a leptomonas or a blastocrithidia?]. Parazitologiia. 2007;41(2): 126–36. (in Russian). PubMed

Maslov DA, Yurchenko VY, Jirků M, Lukeš J. Two new species of trypanosomatid parasites isolated from Heteroptera in Costa Rica. J Eukaryot Microbiol. 2010;57(2): 177–88. 10.1111/j.1550-7408.2009.00464.x PubMed DOI

Dias Fde A, Vasconcellos LR, Romeiro A, Attias M, Souto-Padron TC, Lopes AH. Transovum transmission of trypanosomatid cysts in the Milkweed bug, Oncopeltus fasciatus. PLoS One. 2014;9(9): e108746 10.1371/journal.pone.0108746 PubMed DOI PMC

Gibbs AJ. Crithidia familiaris n. sp. in Cenaeus carnifex Fabr. (Hemiptera). Parasitology. 1950;40(3–4): 322–7. PubMed

McGhee RB, Cosgrove WB. Biology and physiology of the lower Trypanosomatidae. Microbiol Rev. 1980;44(1): 140–73. PubMed PMC

Frolov AO, Malysheva MN, Ganyukova AI, Yurchenko V, Kostygov AY. Life cycle of Blastocrithidia papi sp. n. (Kinetoplastea, Trypanosomatidae) in Pyrrhocoris apterus (Hemiptera, Pyrrhocoridae). Eur J Protistol. 2017;57: 85–98. 10.1016/j.ejop.2016.10.007 PubMed DOI

Caicedo AM, Gallego G, Munoz JE, Suarez H, Torres AG, Carvajal H, et al. Morphological and molecular description of Blastocrithidia cyrtomeni sp. nov. (Kinetoplastea: Trypanosomatidae) associated with Cyrtomenus bergi Froeschner (Hemiptera: Cydnidae) from Colombia. Mem Inst Oswaldo Cruz. 2011;106(3): 301–7. PubMed

Schaub GA, Pretsch M. Ultrastructural studies on the excystment of Blastocrithidia triatomae (Trypanosomatidae). Trans R Soc Trop Med Hyg. 1981;75(1): 168–71. PubMed

Reduth D, Schaub GA. The ultrastructure of the cysts of Blastocrithidia triatomae Cerisola et al. 1971 (Trypanosomatidae): a freeze-fracture study. Parasitol Res. 1988;74(4): 301–6. PubMed

Schaub GA. Pathogenicity of trypanosomatids on insects. Parasitol Today. 1994;10(12): 463–8. PubMed

Takata CSA, Camargo EP, Milder RV. Encystment and excystment of a trypanosomatid of the genus Leptomonas. Eur J Protistol. 1996;32(1): 90–5.

Frolov AO, Karpov SA. Comparative morphology of kinetoplastids. Tsitologiia. 1995;37(11): 1072–96. PubMed

Mehlhorn H, Schaub GA, Peters W, Haberkorn A. Electron microscopic studies on Blastocrithidia triatomae Cerisola et al. 1971 (Trypanosomatidae). Tropenmed Parasitol. 1979;30(3): 289–300. PubMed

Peng PL-M, Wallace FG. The cultivation of Blastocrithidia triatomae Cerisola et al., 1971. J Protozool. 1981;28(1): 116–8.

Tieszen KL, Molyneux DH, Abdel-Hafez SK. Ultrastructure of cyst formation in Blastocrithidia familiaris in Lygaeus pandurus (Hemiptera: Lygaeidae). Z Parasitenk. 1985;71: 179–88.

Tieszen KL, Molyneux DH, Abdelhafez SK. Host-parasite relationships and cysts of Leptomonas lygaei (Trypanosomatidae) in Lygaeus pandurus (Hemiptera, Lygaeidae). Parasitology. 1989;98: 395–400.

Malysheva MN, Frolov AO, Skarlato SO. [Development of cyst-like cells of the flagellate Leptomonas oncopelti in the midgut of the hemipteran Oncopeltus fasciatus]. Tsitologiia. 2006;48(9): 723–33. (in Russian). PubMed

Frolov AO, Skarlato SO, Shaglina EG. [Morphology of cyst-like cells in the flagellate Leptomonas jaculum]. Tsitologiia. 1991;33(10): 55–8. (in Russian). PubMed

Romeiro A, Sole-Cava A, Sousa MA, de Souza W, Attias M. Ultrastructural and biochemical characterization of promastigote and cystic forms of Leptomonas wallacei n. sp. isolated from the intestine of its natural host Oncopeltus fasciatus (Hemiptera: Lygaeidae). J Eukaryot Microbiol. 2000;47(3): 208–20. PubMed

Frolov AO, Skarlato SO. [Fine structure and mechanisms of adaptation of lower trypanosomatids in Hemiptera]. Tsitologyia. 1995;37(7): 539–60. (in Russian).

Mcghee RB, Hanson WL. Growth and reproduction of Leptomonas oncopelti in milkweed bug, Oncopeltus fasciatus. J Protozool. 1962;9(4): 488–93.

Schaub GA. Parasite-host interrelationships of Blastocrithidia triatomae and triatomines. Mem Inst Oswaldo Cruz. 1988;83 Suppl 1: 622–32. PubMed

Schaub GA, Losch P. Parasite/host-interrelationships of the trypanosomatids Trypanosoma cruzi and Blastocrithidia triatomae and the reduviid bug Triatoma infestans: influence of starvation of the bug. Ann Trop Med Parasitol. 1989;83(3): 215–23. PubMed

Schaub GA, Böker CA, Jensen C, Reduth D. Cannibalism and coprophagy are modes of transmission of Blastocrithidia triatomae (Trypanosomatidae) between triatomines. J Protozool. 1989;36(2): 171–5. PubMed

Schaub GA, Schnitker A. Influence of Blastocrithidia triatomae (Trypanosomatidae) on the reduviid bug Triatoma infestans: alterations in the Malpighian tubules. Parasitol Res. 1988;75(2): 88–97. PubMed

Frolov AO, Malysheva MN, Kostygov AY. [Homoxenous trypanosomatids from true bugs Pyrrhocoris apterus (L.) in the north of the Pskov region]. Parazitologiia. 2014;48(6): 461–71. (in Russian). PubMed

Frolov AO, Malysheva MN, Yurchenko V, Kostygov AY. Back to monoxeny: Phytomonas nordicus descended from dixenous plant parasites. Eur J Protistol. 2016;52: 1–10. 10.1016/j.ejop.2015.08.002 PubMed DOI

Votýpka J, Kostygov AY, Kraeva N, Grybchuk-Ieremenko A, Tesařová M, Grybchuk D, et al. Kentomonas gen. n., a new genus of endosymbiont-containing trypanosomatids of Strigomonadinae subfam. n. Protist. 2014. PubMed

Yurchenko V, Lukeš J, Tesařová M, Jirků M, Maslov DA. Morphological discordance of the new trypanosomatid species phylogenetically associated with the genus Crithidia. Protist. 2008;159(1): 99–114. 10.1016/j.protis.2007.07.003 PubMed DOI

Butenko A, Vieira TDS, Frolov AO, Opperdoes FR, Soares RP, Kostygov AY, et al. Leptomonas pyrrhocoris: genomic insight into parasite's physiology. Curr Genomics. 2018;19(2): 150–6. 10.2174/1389202918666170815143331 PubMed DOI PMC

Lipa JJ. Blastocrithidia raabei sp. п., a flagellate parasite of Mesocerus marginatus L. (Hemiptera: Coreidae) Acta Protozool. 1966;4(3): 19–23.

Smirnoff WA, Lipa JJ. Herpetomonas swainei sp. n., a new flagellate parasite of Neodiprion swainei (Hymenoptera: Tenthredinidae). J Invertebr Pathol. 1970;16(2): 187–95.

Frolov AO. [The life cycle of Leptomonas pyrrhocoris (Kinetoplastida, Trypanosomatidae)]. Zool zhurnal. 1987;66(1): 5–11. (in Russian).

Rowton ED, Lushbaugh WB, Mcghee RB. Ultrastructure of the flagellar apparatus and attachment of Herpetomonas ampelophilae in the gut and Malpighian tubules of Drosophila melanogaster. J Protozool. 1981;28(3): 297–301.

Tieszen KL, Molyneux DH. Morphology and host-parasite relationships of Crithidia flexonema (Trypanosomatidae) in the hindgut and Malpighian tubules of Gerris odontogaster (Hemiptera, Gerridae). J Parasitol. 1989;75(3): 441–8.

Halberg KA, Rainey SM, Veland IR, Neuert H, Dornan AJ, Klambt C, et al. The cell adhesion molecule Fasciclin2 regulates brush border length and organization in Drosophila renal tubules. Nat Commun. 2016;7: 11266 10.1038/ncomms11266 PubMed DOI PMC

Vickerman K. Comparative cell biology of the kinetoplastid flagellates In: Vickerman K, Preston TM, editors. Biology of Kinetoplastida. 1 London: Academic Press; 1976. p. 35–130.

Molyneux DH, Ashford RW. The biology of Trypanosoma and Leishmania, parasites of man and domestic animals. New York: Taylor & Francis; 1983. xi, 294 pp.

Frevert U, Reinwald E. Formation of filopodia in Trypanosoma congolense by crosslinking the variant surface antigen. J Ultrastruct Mol Struct Res. 1988;99(2): 124–36. PubMed

Podlipaev SA, Frolov AO. [Description and laboratory cultivation of Blastocrithidia miridarum sp. n. (Mastigophora, Trypanosomatidae)]. Parazitologiia. 1987;21(4): 545–52. (in Russian).

Neresheimer E. Die Fortpflanzung der Opalinen. Arch Protistenkd. 1907;1(Suppl. 1): 1–42.

Wessenberg H. Studies on the life cycle and morphogenesis of Opalina. Univ Calif Publ Zool. 1961;61(6): 315–69.

Wichterman R. Division and conjugation in Nyctotherus cordiformis (Ehr.) Stein (Protozoa, Ciliata) with special reference to the nuclear phenomena. J Morphol. 1937;60(2): 563–611.

Golikova MN. Morphological and cytochemical study of the life cycle of Nyctotherus cordiformis Stein. Acta Protozool. 1963;1(5): 31–42.

Codreanu R. Sur la phase interne du cycle évolutif de deux formes d’Ophryoglena, infusoires endoparasites des larves d’ephémères. CR Acad Sci, Paris. 1930;190: 1154–7.

Codreanu R. La présence d’Ophryoglena, ciliés endoparasites chez les nymphes de l’ephémère Oligoneuria rhenana Imhoff en France. Ann Protist. 1934;4: 181–3.

Desportes I, Schrevel J. The Gregarines The Early Branching Apicomplexa. Leiden: Brill; 2013. 781 pp.

Nowlin N. Correlation of the life cycle of a parasite with the metamorphosis of its host. J Parasitol. 1922;8(4): 153–60.

Cleveland LR. Correlation between the molting period of cryptocercus and sexuality in its protozoa. J Protozool. 1957;4(3): 168–75.

Dogiel VA. General parasitology. New York: Academic Press; 1966. 516 pp.

Jaskowska E, Butler C, Preston G, Kelly S. Phytomonas: trypanosomatids adapted to plant environments. PLoS Pathog. 2015;11(1): e1004484 10.1371/journal.ppat.1004484 PubMed DOI PMC

Kozminsky E, Kraeva N, Ishemgulova A, Dobáková E, Lukeš J, Kment P, et al. Host-specificity of monoxenous trypanosomatids: statistical analysis of the distribution and transmission patterns of the parasites from Neotropical Heteroptera. Protist. 2015;166(5): 551–68. 10.1016/j.protis.2015.08.004 PubMed DOI

Kaltenpoth M, Winter SA, Kleinhammer A. Localization and transmission route of Coriobacterium glomerans, the endosymbiont of pyrrhocorid bugs. FEMS Microbiol Ecol. 2009;69(3): 373–83. 10.1111/j.1574-6941.2009.00722.x PubMed DOI

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Multiple and frequent trypanosomatid co-infections of insects: the Cuban case study

. 2024 May ; 151 (6) : 567-578. [epub] 20240415

Parasites of firebugs in Austria with focus on the "micro"-diversity of the cosmopolitan trypanosomatid Leptomonas pyrrhocoris

. 2023 Dec 11 ; 123 (1) : 27. [epub] 20231211

The Roles of Mosquitoes in the Circulation of Monoxenous Trypanosomatids in Temperate Climates

. 2022 Nov 11 ; 11 (11) : . [epub] 20221111

Development of two species of the Trypanosoma theileri complex in tabanids

. 2022 Mar 21 ; 15 (1) : 95. [epub] 20220321

Genomics of Trypanosomatidae: Where We Stand and What Needs to Be Done?

. 2021 Sep 02 ; 10 (9) : . [epub] 20210902

Euglenozoa: taxonomy, diversity and ecology, symbioses and viruses

. 2021 Mar ; 11 (3) : 200407. [epub] 20210310

Vickermania gen. nov., trypanosomatids that use two joined flagella to resist midgut peristaltic flow within the fly host

. 2020 Dec 02 ; 18 (1) : 187. [epub] 20201202

If host is refractory, insistent parasite goes berserk: Trypanosomatid Blastocrithidia raabei in the dock bug Coreus marginatus

. 2020 ; 15 (1) : e0227832. [epub] 20200116

Development of Phytomonas lipae sp. n. (Kinetoplastea: Trypanosomatidae) in the true bug Coreus marginatus (Heteroptera: Coreidae) and insights into the evolution of life cycles in the genus Phytomonas

. 2019 ; 14 (4) : e0214484. [epub] 20190403

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...