Development of Monoxenous Trypanosomatids and Phytomonads in Insects

Complete trypanosomatid life cycles have been studied for a handful of species, mainly those medical importance (i.e., Leishmania and Trypanosoma).The vast majority trypanosomatids infect insects the orders Diptera Hemiptera, although representatives at least three additional implicated as specific hosts.While monoxenous develop in insect intestinal tract, some them also live Malpighian tubules, hemolymph, salivary glands.Developmental strategies depend on organization digestive system, feeding habits, their hosts. In this review, we summarize current data development phytomonads various insects. Of these, Hemiptera are main host groups, and, consequently, most available information concerns parasites. Within body, midgut hindgut predominant colonization sites; addition, can invade foregut, and/or glands. Differences structure biology determine variety parasites' developmental transmission strategies. Meanwhile, similar mechanisms used by unrelated trypanosomatids, reflecting limited range options to achieve same goal. Trypanosomatids (Euglenozoa: Kinetoplastea: Trypanosomatidae) obligate parasitic flagellates whose evolution was shaped adaptation animal hosts [1.Maslov D.A. et al.Recent advances research: genome organization, expression, metabolism, taxonomy evolution.Parasitology. 2019; 146: 1-27Crossref PubMed Scopus (84) Google Scholar]. There two notable exceptions: genus Phytomonas adapted vascular plants with phytophagous bugs [2.Jaskowska E. al.Phytomonas: plant environments.PLoS Pathog. 2015; 11e1004484Crossref (52) Scholar,3.Camargo E.P. other parasites fruit.Adv. Parasitol. 1999; 42: 29-112Crossref Scholar], few species (at one which belongs Herpetomonas) switched parasitism macronuclei ciliates [4.Fokin S.I. al.Free-living potential reservoirs eukaryotic parasites: occurrence macronucleus Euplotes encysticus.Parasit. Vectors. 2014; 7: 203Crossref (16) Traditionally, united into nontaxonomic groups based type cycle: undergo complete single individual (predominantly an insect), while dixenous ones require distinct hosts, functions vector is typically insect, another vertebrate or [5.Maslov al.Diversity phylogeny trypanosomatids: all that hidden shall be revealed.Trends 2013; 29: 43-52Abstract Full Text PDF (149) Phylogenic inferences convincingly demonstrated independent transitions dixeny Trypanosomatidae [6.Lukeš J. al.Trypanosomatids much more than just trypanosomes: clues from expanded family tree.Trends 2018; 34: 466-480Abstract (99) Despite apparent differences, border between aforementioned not impenetrable. Secondary monoxeny described nordicus, parasite predatory bugs, does [7.Frolov A.O. al.Back monoxeny: nordicus descended parasites.Eur. Protistol. 2016; 52: 1-10Crossref (22) Trypanosoma brucei equiperdum, completely direct [8.Lai D.H. al.Adaptations gradual loss kinetoplast DNA: equiperdum evansi petite mutants T. brucei.Proc. Natl Acad. Sci. U. S. A. 2008; 105: 1999-2004Crossref (195) number recognized suspected agents opportunistic infections [9.Fiorini J.E. al.Morphological, biochemical molecular characterization Herpetomonas samuelpessoai camargoi n. subsp., isolated flower squash Cucurbita moschata.J. Eukaryot. Microbiol. 2001; 48: 62-69Crossref (18) Scholar,10.Conchon I. al.Trypanosomatids, spp., cultured fruit.J. Protozool. 1989; 36: 412-414Crossref (50) Scholar] vertebrates, including humans [11.Kraeva N. al.Leptomonas seymouri: adaptations cycle analyzed sequencing, transcriptome profiling co-infection donovani.PLoS 11e1005127Crossref (77) Scholar,12.Maruyama S.R. al.Non-Leishmania fatal visceral leishmaniasis–like disease, Brazil.Emerg. Infect. Dis. 25: 2088-2092Crossref Currently unites 24 genera, 19 (Figure 1). The present classification system still far perfect reflect true diversity group: genera (Crithidia Leptomonas) monophyletic, (Borovskyia, Lafontella, Lotmaria, Kentomonas, Novymonas, Paratrypanosoma, Sergeia) contain only whereas several unnamed lineages known sequences [13.Kostygov A.Y. Euglenozoa: taxonomy, ecology, symbioses viruses.Open Biol. 2021; 11200407Crossref (35) past, reisolated methods thus far. All these factors render any generalization preliminary point. However, growing gap 'premolecular era' obtained rapidly developing modern techniques must addressed before it becomes too wide. Since spp. fairly well studied, important pathogens (Box 1), focused review (Phytomonas spp.).Box 1Overview Life Cycles spp.Trypanosoma cruziTriatomine infected mammals obtain trypomastigotes amastigotes blood. bug midgut, transform amastigotes, proliferate epimastigotes. latter proliferate, reach brush border, attaching unmodified flagellum. Eventually, they appear rectum, rectal pads' cuticle metacyclic (infective, nondividing) trypomastigotes, discharged feces. They cause infection mammal when getting onto mucosal surface wound caused bug's bite [99.Kollien A.H. Schaub G.A. cruzi Triatominae.Parasitol. Today. 2000; 16: 381-387Abstract (244) Scholar].Salivarian spp.During bloodsucking, tsetse flies acquire bloodstream-form replicative procyclic (e.g., brucei, congolense). After migration anteriorly through proventriculus glands (T. brucei), proboscis hypopharynx congolense), attach via lateral flagellar epithelium cuticular lining, respectively, multiply Finally, injected saliva during blood [100.Peacock L. al.The (Nannomonas) congolense fly.Parasit. 2012; 5: 109Crossref (54) vivax completes its mouthparts stage.Trypanosoma rangeliTrypomastigotes mammalian get triatomine bug, epimastigotes, multiply. Epimastigotes disrupt wall migrate then traverse glands' vacuoles. glands, epithelial divide, eventually free-swimming [101.Garcia E.S. al.Parasite-mediated interactions within vector: rangeli strategies.Parasit. 105Crossref (23) Scholar].Trypanosoma lewisiWhen rats, fleas ingest trypomastigotes. These epitheliocytes inside parasitophorous disruption cells, released either new rectum feces [102.Molyneux Intracellular stages lewisi attempts find such trypanosome species.Parasitology. 1969; 59: 737-744Crossref (17) Scholar].Leishmania spp.Sandflies vertebrates macrophages amastigotes. promastigotes, multiplying bloodmeal surrounded peritrophic matrix, starts decaying posterior end digestion completes. Then promastigotes become active, escape ectoperitrophic space, inserting flagella microvilli, proliferate. Later, anterior where extended tip stomodeal valve destroy chitinase. Others produce proteophosphoglycan gel, encloses vertebrate-infective regurgitated sandfly bloodstream vertebrate, causing [55.Dostálová Volf P. sand flies: parasite-vector overview.Parasit. 276Crossref (178) A mechanism has proposed exist mosquito-transmitted avian trypanosomes [103.Volf al.Blocked models.Int. 2004; 1221-1227Crossref (53) Triatomine Salivarian During stage. Trypomastigotes When Sandflies Exceptional evolutionary plasticity allowed colonize ecological niches, usually dominate, terms both biomass [14.Basset Y. al.Arthropod tropical forest.Science. 338: 1481-1484Crossref (327) Consequently, diverse successful good example case. Regardless whether transmitted external environment (monoxenous species) directly different (dixenous species), exceptions, infective pass possible (see Glossary). Specificity, case, result action coevolutionary forces upon particular [15.Frolov (Kinetoplastea: Trypanosomatida) (Insecta): patterns co-evolution diversification host–parasite systems.Proc. Zool. Inst. RAS. 320 (in Russian): 16-75Google Experimental confirmations required assess reliably, but studies implemented approach so Thus, Crithidia bombi, bumblebee Bombus lucorum, C. mellificae honeybee Apis mellifera, bees families, cross-infections were unsuccessful [16.Ngor al.Cross-infectivity honey bumble bee-associated across bee families.Parasitology. 2020; 147: 1290-1304Crossref (19) Interestingly, parasite, Lotmaria passim, strictly confined host, mellifera [17.Schwarz R.S. al.Characterization mellifera: Langridge McGhee, passim gen., sp.J. 62: 567-583Crossref (113) dipteran Jaenimonas drosophilae, inhabiting Drosophila falleni, larvae successfully overcome metamorphosis [18.Hamilton P.T. al.Infection dynamics immune response newly Drosophila-trypanosomatid association.mBio. 6e01356-15Crossref (30) blow (Calliphoridae) shown flagellate Vickermania spadyakhi, ensign fly Nemopoda nitidula (Sepsidae), horizontally individuals Lucilia sericata, merely survives Calliphora vicina [19.Kostygov al.Vickermania gen. nov., use joined resist peristaltic flow host.BMC 18: 187Crossref (11) examples cannot draw comprehensive picture suggest do universal strategy respect specificity. Assessing further complicated tendency nonspecific facultative An serving carrier bombi bumblebees [20.Ruiz-González M.X. Brown M.J.F. Honey specificity transmission.Ecol. Entomol. 2006; 31: 616-622Crossref (46) For secondarily shield Troilus luridus Picromerus bidens Scholar,21.Ganyukova A.I. al.A novel endosymbiont-containing borealis sp. (Heteroptera: Pentatomidae).Folia 67: 004Google former, hibernating imaginal stage latter, overwintering parasite-free egg, facultative. note, phytomonads, (vectors) unknown, making impossible judge alternative analyzing prevalence populations given [22.Votýpka al.New approaches systematics Trypanosomatidae: criteria taxonomic (re)description.Trends 460-469Abstract (69) While same, high certain may indicate nature relationship. necessary take account issues pitfalls, specimens lead rates [23.Kozminsky al.Host-specificity statistical analysis distribution Neotropical Heteroptera.Protist. 166: 551-568Crossref (24) Scholar,24.Králová al.Insect Papua New Guinea: endemism diversity.Int. 49: 1075-1086Crossref (9) Although nominal almost doubled over past decades had very little impact global preference Insect significantly prevail, followed Hymenoptera, Siphonaptera Blattodea recently added list [25.Yurchenko V. cockroaches description tarakana n.J. 63: 198-209Crossref (29) It remains confirmed Lepidoptera, Trichoptera, Mecoptera, Phthiraptera, previously recorded specifically. 300 typing units (TUs) identified biodiversity assays, reflects rather experimental bias real since Hemipterans 13 cyst-forming (Blastocrithidia Obscuromonas) order Borovskyia barvae symbiont-containing Novymonas esmeraldas members herbivorous families Miridae Rhopalidae, respectively [26.Maslov al.Two Heteroptera Costa Rica.J. 2010; 57: 177-188Crossref (49) Scholar, 27.Kostygov al.Novel trypanosomatid–bacterium association: endosymbiosis action.mBio. 7e01985-15Crossref (48) 28.Kostygov Yurchenko Revised subfamily Leishmaniinae (Trypanosomatidae).Folia 2017; 64: 020Crossref (43) Flagellates Angomonas, Crithidia, Herpetomonas, Leptomonas, Strigomonas, Wallacemonas, Zelonia documented exchange predation copro-/necrophagy transient acquisition seeming likely Scholar,29.Borghesan T.C. al.Molecular phylogenetic redefinition (Kinetoplastea, Trypanosomatidae), associated flies.Protist. 164: 129-152Crossref (65) Scholar,30.Tý? al.Growing (Diptera: Brachycera): frequent cosmopolitism moderate specificity.Mol. Phylogenet. Evol. 69: 255-264Crossref (36) widespread Palearctic brevicula appears generalist capable infecting Nabidae, Gerridae, (nonpredatory) [31.Kostygov revision Wallaceina.Protist. 165: 594-604Crossref dipterans: mosquitoes Culex Calliphoridae, Muscidae, Heleomyzidae, Sepsidae, Antomyidae [32.Schoener al.Trypanosomatid Austrian mosquitoes.PLoS One. 13e0196052Crossref (12) Scholar,33.Ganyukova al.Geographical (Frolov Malysheva, 1989) northern regions Eurasia.Protistology. 14: 70-78Google Out (over 50 TUs), 6 exclusively insects: Jaenimonas, Sergeia, 1, Scholar]). Collectively, 90% four (Crithidia, Lotmaria) detected. Only monotypic exclusive Blechomonas, Blechomonas [34.Votýpka parasitizing (Insecta: Siphonaptera) n.Protist. 763-781Crossref (56) Thus far, Dipteran primary hosts: (i) mosquito-infecting Paratrypanosoma confusum represents earliest branch tree [35.Flegontov al.Paratrypanosoma early-branching trypanosomatid.Curr. 23: 1787-1793Abstract Scholar]; (ii) ancient found date detected Early Cretaceous (~100 mya) amber [36.Poinar Jr., G. Poinar R. Evidence vector-borne disease reptiles.Vector Borne Zoon. 4: 281-284Crossref (32) Scholar,37.Poinar Panstrongylus hispaniolae (Hemiptera: Reduviidae: Triatominae), fossil Dominican amber, evidence gut flagellates.Palaeodiversity. 6: 1-8Google (iii) Adaptation occurred horizontal transfer. As mentioned previously, Notably, one-third localization 2). By 'localization' mean ability form stable, spatially proliferating micropopulations organs tissues [38.Frolov al.Transformations history trypanosomatids. Macrotransformations.Parazitologiia. 49 233-256PubMed Scholar,39.Frolov Trypanosomatidae. Exotransformations.Parazitologiia. 313-338PubMed discrete, gradually change. Monoxenous parasitize insects, divided (foregut), middle (midgut), (hindgut) sections 2A). parts, covered cuticles, food digested nutrients absorbed, bears microvilli apical (also tubules glands). Various structures formed play role