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

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid30943229

Here we described a new trypanosomatid species, Phytomonas lipae, parasitizing the dock bug Coreus marginatus based on axenic culture and in vivo material. Using light and electron microscopy we characterized the development of this flagellate in the intestine, hemolymph and salivary glands of its insect host. The intestinal promastigotes of Phytomonas lipae do not divide and occur only in the anterior part of the midgut. From there they pass into hemolymph, increasing in size, and then to salivary glands, where they actively proliferate without attachment to the host's epithelium and form infective endomastigotes. We conducted molecular phylogenetic analyses based on 18s rRNA, gGAPDH and HSP83 gene sequences, of which the third marker performed the best in terms of resolving phylogenetic relationships within the genus Phytomonas. Our inference demonstrated rather early origin of the lineage comprising the new species, right after that of P. oxycareni, which represents the earliest known branch within the Phytomonas clade. This allowed us to compare the development of P. lipae and three other Phytomonas spp. in their insect hosts and reconstruct the vectorial part of the life cycle of their common ancestor.

Zobrazit více v PubMed

Maslov DA, Opperdoes FR, Kostygov AY, Hashimi H, Lukeš J, Yurchenko V (2019) Recent advances in trypanosomatid research: genome organization, expression, metabolism, taxonomy and evolution. Parasitology (in press). PubMed

Maslov DA, 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. 10.1016/j.pt.2012.11.001 PubMed DOI

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

Lukeš J, Butenko A, Hashimi H, Maslov DA, Votýpka J, Yurchenko V (2018) Trypanosomatids are much more than just trypanosomes: clues from the expanded family tree. Trends Parasitol 34: 466–480. 10.1016/j.pt.2018.03.002 PubMed DOI

Hoare CA (1972) The trypanosomes of mammals Oxford: Blackwell Scientific Publications. 768 p.

Akhoundi M, Kuhls K, Cannet A, Votýpka J, Marty P, Delaunay P, et al. (2016) A historical overview of the classification, evolution, and dispersion of PubMed DOI PMC

Stevens JR, Gibson WC (1999) The evolution of pathogenic trypanosomes. Cad Saude Publica 15: 673–684. PubMed

Camargo EP (1999) PubMed

Dollet M (1984) Plant diseases caused by flagellate protozoa (

Lafont A (1909) Sur la présence d'un parasite de la classe des flagellés dans Ie latex de I'

Donovan C (1909) Kala-azar in Madras, especially with regard to its connexion with the dog and the bug (

Lafont A (1911) Sur la transmission du

Camargo EP, Kastelein P, Roitman I (1990) Trypanosomatid parasites of plants ( PubMed

Camargo EP, Wallace FG (1994) Vectors of plant parasites of the genus Phytomonas (Protozoa, Zoomastigophora, Kinetoplastida) In: Harris KF, editor. Advances in Disease Vector Research. New York, NY: Springer; pp. 333–359.

Jaskowska E, Butler C, Preston G, Kelly S (2015) PubMed DOI PMC

Serrano MG, Nunes LR, Campaner M, Buck GA, Camargo EP, Teixeira MM (1999) Trypanosomatidae: PubMed DOI

Sturm NR, Fernandes O, Campbell DA (1995) The mini-exon genes of three PubMed DOI

Hollar L, Maslov DA (1997) A phylogenetic view on the genus PubMed

Frolov AO, Malysheva MN, Yurchenko V, Kostygov AY (2016) Back to monoxeny: PubMed DOI

Zanetti A, Ferreira RC, Serrano MG, Takata CS, Campaner M, Attias M, et al. (2016) PubMed DOI

Seward EA, Votýpka J, Kment P, Lukeš J, Kelly S (2017) Description of PubMed DOI

Kořený L, Sobotka R, Kovářová J, Gnipová A, Flegontov P, Horváth A, et al. (2012) Aerobic kinetoplastid flagellate PubMed DOI PMC

Porcel BM, Denoeud F, Opperdoes FR, Noel B, Madoui M-A, Hammarton TC, et al. (2014) The streamlined genome of PubMed DOI PMC

Butler CE, Jaskowska E, Kelly S (2017) Genome sequence of PubMed DOI PMC

Yurchenko V, Kostygov A, Havlová J, Grybchuk-Ieremenko A, Ševčíková T, Lukeš J, et al. (2016) Diversity of trypanosomatids in cockroaches and the description of PubMed DOI

Dollet M, Sturm NR, Sanchez-Moreno M, Campbell DA (2000) 5S ribosomal RNA gene repeat sequences define at least eight groups of plant trypanosomatids ( PubMed

Dollet M, Sturm NR, Campbell DA (2012) The internal transcribed spacer of ribosomal RNA genes in plant trypanosomes ( PubMed DOI

Frolov AO, Malysheva MN (1993) [Description of

Lipa JJ (1966)

Wallace FG (1966) The trypanosomatid parasites of insects and arachnids. Exp Parasitol 18: 124–193. PubMed

Schaub GA (1994) Pathogenicity of trypanosomatids on insects. Parasitol Today 10: 463–468. PubMed

Frolov AO, Skarlato SO (1995) [Fine structure and mechanisms of adaptation of lower trypanosomatids in Hemiptera]. Tsitologiia 37: 539–560. (in Russian).

Frolov AO, Malysheva MN, Ganyukova AI, Yurchenko V, Kostygov AY (2017) Life cycle of PubMed DOI

Podlipaev SA, Frolov AO (1987) [Description and laboratory cultivation of

Votýpka J, Kostygov AY, Kraeva N, Grybchuk-Ieremenko A, Tesařová M, Grybchuk D, et al. (2014) PubMed DOI

Kostygov AY, Grybchuk-Ieremenko A, Malysheva MN, Frolov AO, Yurchenko V (2014) Molecular revision of the genus PubMed DOI

Frolov AO, Malysheva MN, Ganyukova AI, Yurchenko V, Kostygov AY (2018) Obligate development of PubMed DOI PMC

Týč J, Votýpka J, Klepetková H, Šuláková H, Jirků M, Lukeš J (2013) Growing diversity of trypanosomatid parasites of flies (Diptera: Brachycera): frequent cosmopolitism and moderate host specificity. Mol Phylogenet Evol 69: 255–264. 10.1016/j.ympev.2013.05.024 PubMed DOI

Maslov DA, Lukeš J, Jirků M, Simpson L (1996) Phylogeny of trypanosomes as inferred from the small and large subunit rRNAs: implications for the evolution of parasitism in the trypanosomatid protozoa. Mol Biochem Parasitol 75: 197–205. PubMed

Maslov DA, Yurchenko VY, Jirků M, Lukeš J (2010) Two new species of trypanosomatid parasites isolated from Heteroptera in Costa Rica. J Eukaryot Microbiol 57: 177–188. 10.1111/j.1550-7408.2009.00464.x PubMed DOI

Simpson AG, Lukeš J, Roger AJ (2002) The evolutionary history of kinetoplastids and their kinetoplasts. Mol Biol Evol 19: 2071–2083. 10.1093/oxfordjournals.molbev.a004032 PubMed DOI

Gerasimov ES, Kostygov AY, Yan S, Kolesnikov AA (2012) From cryptogene to gene? ND8 editing domain reduction in insect trypanosomatids. Eur J Protistol 48: 185–193. 10.1016/j.ejop.2011.09.002 PubMed DOI

Kostygov A, Dobáková E, Grybchuk-Ieremenko A, Váhala D, Maslov DA, Votýpka J, et al. (2016) Novel trypanosomatid—bacterium association: evolution of endosymbiosis in action. mBio 7: e01985–01915. PubMed PMC

Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Ostell J, Pruitt KD, et al. (2018) GenBank. Nucleic Acids Res 46: D41–D47. 10.1093/nar/gkx1094 PubMed DOI PMC

Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30: 772–780. 10.1093/molbev/mst010 PubMed DOI PMC

Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger satasets. Mol Biol Evol 33: 1870–1874. 10.1093/molbev/msw054 PubMed DOI PMC

Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797. 10.1093/nar/gkh340 PubMed DOI PMC

Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540–552. 10.1093/oxfordjournals.molbev.a026334 PubMed DOI

Chistyakova LV, Kostygov AY, Kornilova OA, Yurchenko V (2014) Reisolation and redescription of PubMed DOI

Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32: 268–274. 10.1093/molbev/msu300 PubMed DOI PMC

Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, et al. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61: 539–542. 10.1093/sysbio/sys029 PubMed DOI PMC

Spodareva VV, Grybchuk-Ieremenko A, Losev A, Votýpka J, Lukeš J, Yurchenko V, et al. (2018) Diversity and evolution of anuran trypanosomes: insights from the study of European species. Parasit Vectors 11: 447 10.1186/s13071-018-3023-1 PubMed DOI PMC

Votýpka J, d'Avila-Levy CM, Grellier P, Maslov DA, Lukeš J, Yurchenko V (2015) New approaches to systematics of Trypanosomatidae: criteria for taxonomic (re)description. Trends Parasitol 31: 460–469. 10.1016/j.pt.2015.06.015 PubMed DOI

Hrušková M, Honěk A, Pekár S (2005)

Kment P, Vahala O, Hradil K (2006) [First records of

Nedvěd O, Chehlarov E, Kalushkov P (2014) Life history of the invasive bug

Jankevicius JV, Jankevicius SI, Campaner M, Conchon I, Maeda LA, Teixeira MMG, et al. (1989) Life cycle and culturing of

Freymuller E, Milder R, Jankevicius JV, Jankevicius SI, Camargo EP (1990) Ultrastructural studies on the trypanosomatid

Frolov AO, Malysheva MN, Kostygov AY (2015) [Transformations of Life Cycles in the Evolutionary History of Trypanosomatids. Macrotransformations]. Parazitologiia 49: 233–256. (in Russian). PubMed

Hecker H, Schwarzenbach M, Rudin W (1990) Development and interactions of PubMed

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...