Leptomonas pyrrhocoris: Genomic insight into Parasite's Physiology

. 2018 Feb ; 19 (2) : 150-156.

Status PubMed-not-MEDLINE Jazyk angličtina Země Spojené arabské emiráty Médium print

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid29491743

BACKGROUND: Leptomonas pyrrhocoris is a parasite of the firebug Pyrrhocoris apterus. This flagellate has been recently proposed as a model species for studying different aspects of the biology of monoxenous trypanosomatids, including host - parasite interactions. During its life cycle L. pyrrhocoris never tightly attaches to the epithelium of the insect gut. In contrast, its dixenous relatives (Leishmania spp.) establish a stable infection via attachment to the intestinal walls of their insect hosts. MATERIAL AND METHODS: This process is mediated by chemical modifications of the cell surface lipophosphoglycans. In our study we tested whether the inability of L. pyrrhocoris to attach to the firebug's midgut is associated with the absence of these glycoconjugates. We also analyzed evolution of the proteins involved in proper lipophosphoglycan assembly, cell attachment and establishment of a stable infection in L. pyrrhocoris, L. seymouri, and Leishmania spp. Our comparative analysis demonstrated differences in SCG/L/R repertoire between the two parasite subgenera, Leishmania and Viannia, which may be related to distinct life strategies in various Leishmania spp. The genome of L. pyrrhocoris encodes 6 SCG genes, all of which are quite divergent from their orthologs in the genus Leishmania. Using direct probing with an antibody recognizing the β-Gal side chains of lipophosphoglycans, we confirmed that these structures are not synthesized in L. pyrrhocoris. CONCLUSION: We conclude that either the SCG enzymes are not active in this species (similarly to SCG5/7 in L. major), or they possess a different biochemical activity.

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Lumsden W.H., Evans D.A. Biology of Kinetoplastida. Vol. 1 London: Academic Press; 1976.

Podlipaev S.A. The more insect trypanosomatids under study - the more diverse Trypanosomatidae appears. Int. J. Parasitol. 2001;31(5-6):648–652. PubMed

Maslov D.A., 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. PubMed

Bacchi J., Lambros C., Goldberg B., Hutner S.H., de Carvalho G.D. Susceptibility of an insect Leptomonas and Crithidia fasciculata to several established antitrypanosomatid agents. Antimicrob. Agents Chemother. 1974;6(6):785–790. PubMed PMC

Hassan H.F., Coombs G.H. A comparative study of the purine- and pyrimidine-metabolising enzymes of a range of trypanosomatids. Comp. Biochem. Physiol. B. 1986;84(2):219–223. PubMed

Schaub G.A., Jensen C. Developmental time and mortality of the reduviid bug Triatoma infestans with differential exposure to coprophagic infections with Blastocrithidia triatomae (Trypanosomatidae). J. Invertebr. Pathol. 1990;55(1):17–27. PubMed

Lukeš J., Skalický T., Týč J., Votýpka J., Yurchenko V. Evolution of parasitism in kinetoplastid flagellates. Mol. Biochem. Parasitol. 2014;195(2):115–122. PubMed

Kozminsky E., Kraeva N., Ishemgulova A., Dobáková E., Lukeš J., Kment P., Yurchenko V., Votýpka J., Maslov D.A. Host-specificity of monoxenous trypanosomatids: Statistical analysis of the distribution and transmission patterns of the parasites from Neotropical Heteroptera. Protist. 2015;166(5):551–568. PubMed

Hamilton P.T., Votýpka J., Dostalova A., Yurchenko V., Bird N.H., Lukeš J., Lemaitre B., Perlman S.J. Infection dynamics and immune response in a newly described Drosophila-trypanosomatid association. MBio. 2015;6(5):e01356–e01315. PubMed PMC

Stuart K., Panigrahi A.K. RNA editing: Complexity and complications. Mol. Microbiol. 2002;45(3):591–596. PubMed

Opperdoes F.R., Butenko A., Flegontov P., Yurchenko V., Lukeš J. Comparative metabolism of free-living Bodo saltans and parasitic trypanosomatids. J. Eukaryot. Microbiol. 2016;63(5):657–678. PubMed

Záhonová K., Kostygov A., Ševčíková T., Yurchenko V., Eliáš M. An unprecedented non-canonical nuclear genetic code with all three termination codons reassigned as sense codons. Curr. Biol. 2016;26(17):2364–2369. PubMed

Fenn K., Matthews K.R. The cell biology of Trypanosoma brucei differentiation. Curr. Opin. Microbiol. 2007;10(6):539–546. PubMed PMC

Clayton J. Chagas disease 101. Nature. 2010;465(7301):S4–S5. https://www.nature.com/articles/nature09220 PubMed

Bates P.A., Rogers M.E. New insights into the developmental biology and transmission mechanisms of Leishmania. Curr. Mol. Med. 2004;4(6):601–609. PubMed

Frolov A.O., Malysheva M.N., Yurchenko V., Kostygov A.Y. 2016 http://www.sciencedirect.com/science/article/pii/S09324739

Jankevicius J.V., Jankevicius S.I., Campaner M., Conchon I., Maeda L.A., Teixeira M.M., Freymuller E., Camargo E.P. Life cycle and culturing of Phytomonas serpens (Gibbs), a trypanosomatid parasite of tomatoes. J. Protozool. 1989;36(3):265–271.

Frolov A.O. The life cycle of Leptomonas pyrrhocoris (Kinetoplastida, Trypanosomatidae). Zool. zhurnal. 1987;66(1):5–11.

Frolov A.O. Life cycle of Blastocrithidia miridarum (Kinetoplastida, Trypanosomatidae). Zool. zhurnal. 1987;66(5):655–661.

Mehlhorn H., Schaub G.A., Peters W., Haberkorn A. 1971 (Trypanosomatidae). Tropenmed. Parasitol. 1979;30(3):289–300. PubMed

Alcolea P.J., Alonso A., Garcia-Tabares F., Torano A., Larraga V. An insight into the proteome of Crithidia fasciculata choanomastigotes as a comparative approach to axenic growth, peanut lectin agglutination and differentiation of Leishmania spp. promastigotes. PLoS One. 2014;9(12):e113837. journals.plos.org/plosone/article?id=10.1371/journal.pone.0113837 PubMed PMC

Frolov A.O., Malysheva M.N., Ganyukova A.I., Yurchenko V., Kostygov A.Y. Life cycle of Blastocrithidia papi sp. n. (Kinetoplastea, Trypanosomatidae) in Pyrrhocoris apterus (Hemiptera, Pyrrhocoridae). Eur. J. Protistol. 2017;57:85–98. http://www.sciencedirect.com/science/article/pii/S0932473916301249 PubMed

Frolov A.O., Skarlato S.O. Fine structure and mechanisms of adaptation of lower trypanosomatids in Hemiptera. Tsitologiia. 1995;37(7):539–560.

Frolov A.O., Malysheva M.N., Kostygov A.Y. Homoxenous trypanosomatids from true bugs Pyrrhocoris apterus (L.) in the North of the Pskov region. Parazitologiia. 2014;48(6):461–471. PubMed

Teodoro G. Osservazioni sul Pyrrhocoris apterus L., con particolare riguardo alla flagellosi. Redia (Firenze) 1927;16:45–50.

Flegontov P., Butenko A., Firsov S., Kraeva N., Eliáš M., Field M.C., Filatov D., Flegontova O., Gerasimov E.S., Hlaváčová J., Ishemgulova A., Jackson A.P., Kelly S., Kostygov A., Logacheva M.D., Maslov D.A., Opperdoes F.R., O’Reilly A., Sádlová J., Ševčíková T., Venkatesh D., Vlček Č., Volf P., Votýpka J., Záhonová K., Yurchenko V., Lukeš J. Genome of Leptomonas pyrrhocoris: A high-quality reference for monoxenous trypanosomatids and new insights into evolution of Leishmania. Sci. Rep. 2016;6:23704. https://www.nature.com/ articles/srep23704 PubMed PMC

Cantacessi C., Dantas-Torres F., Nolan M.J., Otranto D. The past, present, and future of Leishmania genomics and transcriptomics. Trends Parasitol. 2015;31(3):100–108. PubMed PMC

Kraeva N., Butenko A., Hlaváčová J., Kostygov A., Myškova J., Grybchuk D., Leštinová T., Votýpka J., Volf P., Opperdoes F., Flegontov P., Lukeš J., Yurchenko V. Leptomonas seymouri. 2015 journals.plos.org/plospathogens/article?id=10.1371/journal.ppat PubMed PMC

Singh N., Chikara S., Sundar S. SOLiD sequencing of genomes of clinical isolates of Leishmania donovani from India confirm Leptomonas co-infection and raise some key questions. PLoS One. 2013;8(2):e55738. journals.plos.org/plosone /article?id=10.1371/journal.pone.0055738 PubMed PMC

Ghosh S., Banerjee P., Sarkar A., Datta S., Chatterjee M. Coinfection of Leptomonas seymouri and Leishmania donovani in Indian leishmaniasis. J. Clin. Microbiol. 2012;50(8):2774–2778. PubMed PMC

Fernandes A.P., Nelson K., Beverley S.M. Evolution of nuclear ribosomal RNAs in kinetoplastid protozoa: Perspectives on the age and origins of parasitism. Proc. Natl. Acad. Sci. USA. 1993;90(24):11608–11612. PubMed PMC

Jirků M., Yurchenko V.Y., Lukeš J., Maslov D.A. New species of insect trypanosomatids from Costa Rica and the proposal for a new subfamily within the Trypanosomatidae. J. Eukaryot. Microbiol. 2012;59(6):537–547. PubMed

Spath G.F., Epstein L., Leader B., Singer S.M., Avila H.A., Turco S.J., Beverley S.M. Lipophosphoglycan is a virulence factor distinct from related glycoconjugates in the protozoan parasite Leishmania major. Proc. Natl. Acad. Sci. USA. 2000;97(16):9258–9263. PubMed PMC

Kamhawi S., Ramalho-Ortigao M., Pham V.M., Kumar S., Lawyer P.G., Turco S.J., Barillas-Mury C., Sacks D.L., Valenzuela J.G. A role for insect galectins in parasite survival. Cell. 2004;119(3):329–341. PubMed

Dostálová A., Volf P. Leishmania development in sand flies: Parasite-vector interactions overview. Parasit. Vectors. 2012;5:276. http://www.academia.edu/28877718/ [Leishmania_development _in_sand_flies_parasite-vector_interactions_overview]. PubMed PMC

El-Sayed N.M., Myler P.J., Blandin G., Berriman M., Crabtree J., Aggarwal G., Caler E., Renauld H., Worthey E.A., Hertz-Fowler C., Ghedin E., Peacock C., Bartholomeu D.C., Haas B.J., Tran A.N., Wortman J.R., Alsmark U.C., Angiuoli S., Anupama A., Badger J., Bringaud F., Cadag E., Carlton J.M., Cerqueira G.C., Creasy T., Delcher A.L., Djikeng A., Embley T.M., Hauser C., Ivens A.C., Kummerfeld S.K., Pereira-Leal J.B., Nilsson D., Peterson J., Salzberg S.L., Shallom J., Silva J.C., Sundaram J., Westenberger S., White O., Melville S.E., Donelson J.E., Andersson B., Stuart K.D., Hall N. Comparative genomics of trypanosomatid parasitic protozoa. Science. 2005;309(5733):404–409. science.sciencemag.org /content/sci/309/5733/404.full.pdf PubMed

McConville M.J., Turco S.J., Ferguson M.A., Sacks D.L. Developmental modification of lipophosphoglycan during the differentiation of Leishmania major promastigotes to an infectious stage. EMBO J. 1992;11(10):3593–3600. PubMed PMC

Sacks D.L., Pimenta P.F., McConville M.J., Schneider P., Turco S.J. Stage-specific binding of Leishmania donovani to the sand fly vector midgut is regulated by conformational changes in the abundant surface lipophosphoglycan. J. Exp. Med. 1995;181(2):685–697. PubMed PMC

Soares R.P., Macedo M.E., Ropert C., Gontijo N.F., Almeida I.C., Gazzinelli R.T., Pimenta P.F., Turco S.J. Leishmania chagasi: lipophosphoglycan characterization and binding to the midgut of the sand fly vector Lutzomyia longipalpis. Mol. Biochem. Parasitol. 2002;121(2):213–224. PubMed

Soares R.P., Cardoso T.L., Barron T., Araujo M.S., Pimenta P.F., Turco S.J. Leishmania braziliensis: A novel mechanism in the lipophosphoglycan regulation during metacyclogenesis. Int. J. Parasitol. 2005;35(3):245–253. PubMed

de Assis R.R., Ibraim I.C., Nogueira P.M., Soares R.P., Turco S.J. Glycoconjugates in New World species of Leishmania: Polymorphisms in lipophosphoglycan and glycoinositolphospholipids and interaction with hosts. Biochim. Biophys. Acta. 2012;1820(9):1354–1365. PubMed

Volf P., Nogueira P.M., Myšková J., Turco S.J., Soares R.P. Structural comparison of lipophosphoglycan from Leishmania turanica and L. major, two species transmitted by Phlebotomus papatasi. Parasitol. Int. 2014;63(5):683–686. PubMed

Sacks D.L., Saraiva E.M., Rowton E., Turco S.J., Pimenta P.F. The role of the lipophosphoglycan of Leishmania in vector competence. Parasitology. 1994;108(Suppl.):S55–S62. journals.cambridge.org/article_S0031182000075727 PubMed

Dobson D.E., Scholtes L.D., Myler P.J., Turco S.J., Beverley S.M. Genomic organization and expression of the expanded SCG/L/R gene family of Leishmania major: Internal clusters and telomeric localization of SCGs mediating species-specific LPG modifications. Mol. Biochem. Parasitol. 2006;146(2):231–241. PubMed

Dobson D.E., Scholtes L.D., Valdez K.E., Sullivan D.R., Mengeling B.J., Cilmi S., Turco S.J., Beverley S.M. Functional identification of galactosyltransferases (SCGs) required for species-specific modifications of the lipophosphoglycan adhesin controlling Leishmania major-sand fly interactions. J. Biol. Chem. 2003;278(18):15523–15531. PubMed

Malysheva M.N., Mamkaeva M.A., Kostygov A.Y., Frolov A.O., Karpov S.A. Culture collection of parasitic protists at the Zoological Institute RAS (CCPP ZIN RAS). Protistology. 2016;10(1):26–42.

Kostygov A.Y., Grybchuk-Ieremenko A., Malysheva M.N., Frolov A.O., Yurchenko V. Molecular revision of the genus Wallaceina. Protist. 2014;165(5):594–604. PubMed

Dobson D.E., Kamhawi S., Lawyer P., Turco S.J., Beverley S.M., Sacks D.L. Leishmania major survival in selective Phlebotomus papatasi sand fly vector requires a specific SCG-encoded lipophosphoglycan galactosylation pattern. PLoS Pathog. 2010;6(11):e1001185. journals.plos.org/plospathogens/ article?id=10.1371/journal.ppat.1001185 PubMed PMC

Peacock C.S., Seeger K., Harris D., Murphy L., Ruiz J.C., Quail M.A., Peters N., Adlem E., Tivey A., Aslett M., Kerhornou A., Ivens A., Fraser A., Rajandream M.A., Carver T., Norbertczak H., Chillingworth T., Hance Z., Jagels K., Moule S., Ormond D., Rutter S., Squares R., Whitehead S., Rabbinowitsch E., Arrowsmith C., White B., Thurston S., Bringaud F., Baldauf S.L., Faulconbridge A., Jeffares D., Depledge D.P., Oyola S.O., Hilley J.D., Brito L.O., Tosi L.R., Barrell B., Cruz A.K., Mottram J.C., Smith D.F., Berriman M. Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat. Genet. 2007;39(7):839–847. PubMed PMC

Edgar R.C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–1797. PubMed PMC

Talavera G., Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst. Biol. 2007;56(4):564–577. PubMed

Trifinopoulos J., Nguyen L.T., von Haeseler A., Minh B.Q. W-IQ-TREE: A fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res. 2016;44(W1):W232-235. PubMed PMC

Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Hohna S., Larget B., Liu L., Suchard M.A., Huelsenbeck J.P. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 2012;61(3):539–542. PubMed PMC

Wu A.C., Freitas M.A., Silva Sde O., Nogueira P.M., Soares R.P., Pesquero J.B., Gomes M.A., Pesquero J.L., Melo M.N. Genetic differences between two Leishmania major-like strains revealed by suppression subtractive hybridization. Mol. Biochem. Parasitol. 2015;203(1-2):34–38. PubMed

Mookherjee N., Pearson T.W. Trypanosoma simiae and Trypanosoma congolense: Surface glycoconjugates of procyclic forms-the same coats on different hangers? Exp. Parasitol. 2002;100(4):257–268. PubMed

Kelleher M., Bacic A., Handman E. Identification of a macrophage-binding determinant on lipophosphoglycan from Leishmania major promastigotes. Proc. Natl. Acad. Sci. USA. 1992;89(1):6–10. PubMed PMC

Soares R.P., Margonari C., Secundino N.C., Macedo M.E., da Costa S.M., Rangel E.F., Pimenta P.F., Turco S.J. 2010 https://www.hindawi.com/journals/bmri/2010/439174/abs/ PubMed PMC

Sacks D.L., Modi G., Rowton E., Spath G., Epstein L., Turco S.J., Beverley S.M. The role of phosphoglycans in Leishmania-sand fly interactions. Proc. Natl. Acad. Sci. USA. 2000;97(1):406–411. PubMed PMC

Dobson D.E., Mengeling B.J., Cilmi S., Hickerson S., Turco S.J., Beverley S.M. Identification of genes encoding arabinosyltransferases (SCA) mediating developmental modifications of lipophosphoglycan required for sand fly transmission of Leishmania major. J. Biol. Chem. 2003;278(31):28840–28848. PubMed

Lainson R., Ward R.D., Shaw J.J. Leishmania in phlebotomid sandflies: VI. Importance of hindgut development in distinguishing between parasites of the Leishmania mexicana and L. braziliensis complexes. Proc. R. Soc. Lond. B Biol. Sci. 1977;199(1135):309–320. rspb.royalsocietypublishing.org/content/199/1135/309 PubMed

Mahoney A.B., Sacks D.L., Saraiva E., Modi G., Turco S.J. Intra-species and stage-specific polymorphisms in lipophosphoglycan structure control Leishmania donovani-sand fly interactions. Biochemistry. 1999;38(31):9813–9823. PubMed

Coelho-Finamore J.M., Freitas V.C., Assis R.R., Melo M.N., Novozhilova N., Secundino N.F., Pimenta P.F., Turco S.J., Soares R.P. Leishmania infantum: Lipophosphoglycan intraspecific variation and interaction with vertebrate and invertebrate hosts. Int. J. Parasitol. 2011;41(3-4):333–342. PubMed

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