Free-living ciliates as potential reservoirs for eukaryotic parasites: Occurrence of a trypanosomatid in the macronucleus of Euplotes encysticus

Parasites and Vectors

Volumn 7, Issue 1, 2014, Pages

  Fokin, Sergei I ^a,b   Schrallhammer, Martina ^c,d   Chiellini, Carolina ^a,e   Verni, Franco ^a   Petroni, Giulio ^a  

^a UNIVERSITY OF PISA   (Italy)

^b ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

^c UNIVERSITY OF FREIBURG   (Germany)

^d DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^e ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

Author keywords

Ciliophora; Endosymbiont; Euplotes encysticus; Herpetomonas; Host range; Leptomonas; Macronucleus; Parasite; Phytomonas; Protozoa

Indexed keywords

FRESH WATER; RNA 18S;

ARTICLE; CELL STRUCTURE; CERATOPOGONIDAE; CILIATE; CONTROLLED STUDY; CULICOIDES; CULICOIDES KIBUNENSIS; CULICOIDES TRUNCORUM; EUPLOTES ENCYSTICUS; FLUORESCENCE MICROSCOPY; GENE IDENTIFICATION; GENE SEQUENCE; GROWTH RATE; HERPETOMONAS TRIMORPHA; HERPETOMONAS ZTIPLIKA; KINETOPLASTIDA; LIGHT; MACRONUCLEUS; MORPHOLOGICAL TRAIT; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE LOCALIZATION; PHYLOGENY; PROTOZOON; RESERVOIR; TRANSMISSION ELECTRON MICROSCOPY; TRYPANOSOMATID INFECTION; ANIMAL; CLASSIFICATION; DISEASE CARRIER; EUPLOTES; GENETICS; HOST PARASITE INTERACTION; ISOLATION AND PURIFICATION; PARASITOLOGY;

CERATOPOGONIDAE; CILIOPHORA; CULICOIDES KIBUNENSIS; DIPTERA; EUKARYOTA; EUPLOTES; HEMIPTERA; HERPETOMONAS; HERPETOMONAS ZTIPLIKA; HEXAPODA; KINETOPLASTIDA; LEPTOMONAS; MASTIGOPHORA (FLAGELLATES); PHYTOMONAS; PROTISTA; PROTOZOA; TRIMORPHA; TRYPANOSOMATIDAE;

ANIMALS; DISEASE RESERVOIRS; EUPLOTES; HOST-PARASITE INTERACTIONS; MACRONUCLEUS; PHYLOGENY; RNA, RIBOSOMAL, 18S; TRYPANOSOMATINA;

EID: 84900501626     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/1756-3305-7-203     Document Type: Article

References (53)

1. Diversity and phylogeny of insect trypanosomatids: all that is hidden shall be revealed. Maslov DA, Votýpka J, Yurchenko V, Lukeš J, Trends Parasitol 2013 29 43 52 10.1016/j.pt.2012.11.001 23246083
2. Insect trypanosomatids: the need to know more. Podlipaev SA, Mem Inst Oswaldo Cruz 2000 95 517 522 10.1590/S0074-02762000000400013 10904409
3. Probing into the diversity of trypanosomatid flagellates parasitizing insect hosts in South-West China reveals both endemism and global dispersal. Votýpka J, Maslov DA, Yurchenko V, Jirků M, Kment P, Lun Z-R, Lukeš J, Mol Phylogenet Evol 2010 54 243 253 10.1016/j.ympev.2009.10.014 19835965
4. Growing diversity of trypanosomatid parasites of flies (Diptera: Brachycera): Frequent cosmopolitism and moderate host specificity. Týč J, Votýpka J, Klepetková H, Sulá ková H, Jirků M, Lukeš J, Mol Phylogenet Evol 2013 69 255 264 10.1016/j.ympev.2013.05.024 23747522
5. Molecular phylogenetic redefinition of Herpetomonas (Kinetoplastea, Trypanosomatidae), a genus of insect parasites associated with flies. Borghesan TC, Ferreira RC, Takata CSA, Campaner M, Borda CC, Paiva F, Milder RV, Teixeira MMG, Camargo EP, Protist 2013 164 129 152 10.1016/j.protis.2012.06.001 22938923
6. Diversity of insect trypanosomatids assessed from the spliced leader RNA and 5S rRNA genes and intergenic regions. Podlipaev SA, Sturm NR, Fiala I, Fernandes O, Westenberger S, Dollet M, Campbell D, Lukes J, J Eukaryot Microbiol 2004 51 283 290 10.1111/j.1550-7408.2004.tb00568.x 15218696 (Pubitemid 38689119)
7. Cosmopolitan distribution of a trypanosomatid Leptomonas pyrrhocoris. Votýpka J, Klepetková H, Yurchenko VY, Horák A, Lukeš J, Maslov DA, Protist 2012 163 616 631 10.1016/j.protis.2011.12.004 22341645
8. Herpetomonas ztiplika n. Sp. (Kinetoplastida: Trypanosomatidae): a parasite of the blood-sucking biting midge Culicoides kibunensis Tokunaga, 1937 (Diptera: Ceratopogonidae). Podlipaev SA, Votýpka J, Jirků M, Svobodová M, Lukes J, J Parasitol 2004 90 342 347 10.1645/GE-156R 15165057 (Pubitemid 38621340)
9. Herpetomonas trimorpha sp. Nov. (Trypanosomatidae, Kinetoplastida), a parasite of the biting midge Culicoides truncorum (Ceratopogonidae, Diptera). Zídková L, Cepicka I, Votypka J, Svobodová M, Int J Syst Evol Microbiol 2010 60 2236 2246 10.1099/ijs.0.014555-0 19819998
10. Diversity of Trypanosomatids (Kinetoplastea: Trypanosomatidae) parasitizing fleas (Insecta: Siphonaptera) and description of a new genus Blechomonas gen. N. Votypka J, Suková E, Kraeva N, Ishemgulova A, Dǔ I, Yurchenko V, Luke J, Proti 2013 164 763 781 10.1016/j.protis.2013. 08.002
11. A new lineage of trypanosomes from Australian vertebrates and terrestrial bloodsucking leeches (Haemadipsidae). Hamilton PB, Stevens JR, Gidley J, Holz P, Gibson WC, Int J Parasitol 2005 35 431 443 10.1016/j.ijpara.2004.12.005 15777919 (Pubitemid 40381161)
12. 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. Teixeira MMG, Borghesan TC, Ferreira RC, Santos MA, Takata CSA, Campaner M, Nunes VLB, Milder RV, de Souza W, Camargo EP, Protist 2011 162 503 524 10.1016/j.protis.2011.01. 001 21420905
13. Sergeia podlipaevi gen. Nov., sp. Nov. (Trypanosomatidae, Kinetoplastida), a parasite of biting midges (Ceratopogonidae, Diptera). Svobodová M, Zídková L, Cepicka I, Oborník M, Lukes J, Votýpka J, Int J Syst Evol Microbiol 2007 57 Pt 2 423 432 17267991
14. Demonstration that Leptomonas pessoai Galvão, Oliveira, Carvalho & Veiga, 1970, is a Herpetomonas. Roitman I, Brener Z, Roitman C, Kitajima E, J Protozool 1976 23 291 293 10.1111/j.1550-7408.1976.tb03773.x 933085
15. Morphological, biochemical and molecular characterization of Herpetomonas samuelpessoai camargoi n. Subsp., a trypanosomatid isolated from the flower of the squash Cucurbita moschata. Fiorini J, Takata C, Teofilo V, Nascimento L, Faria-e-Silva P, Soares M, Teixeira M, De Souza W, J Eukaryot Microbiol 2001 48 62 69 10.1111/j.1550-7408.2001.tb00416.x 11249194 (Pubitemid 32180370)
16. Herpetomonas spp. Isolated from tomato fruits (Lycopersicon esculentum) in southern Spain. Marín C, Fabre S, Sánchez-Moreno M, Dollet M, Exp Parasitol 2007 116 88 90 10.1016/j.exppara.2006.11.003 17266953 (Pubitemid 46412313)
17. Isolation of a protozoan parasite genetically related to the insect trypanosomatid Herpetomonas samuelpessoai from a human immunodeficiency virus-positive patient. Morio F, Reynes J, Dollet M, Pratlong F, Dedet J-P, Ravel C, J Clin Microbiol 2008 46 3845 3847 10.1128/JCM.01098-08 18832132
18. Ciliatosporidium platyophryae nov. gen., nov. Spec. (Microspora incerta sedis), a parasite of Platyophrya terricola (Ciliophora, Colpodea). Foissner I, Foissner W, Eur J Protistol 1995 31 248 259 10.1016/S0932-4739(11)80088-X
19. Euplotespora binucleata n. gen., n. Sp. (Protozoa: Microsporidia), a parasite infecting the hypotrichous ciliate Euplotes woodruffi, with observations on microsporidian infections in ciliophora. Fokin SI, Di Giuseppe G, Erra F, Dini F, J Eukaryot Microbiol 2008 55 214 228 10.1111/j.1550-7408. 2008.00322.x 18460159 (Pubitemid 351629915)
20. A new species of Leptomonas parasitizing the macronucleus of Paramecium trichium. Gillies C, Hanson ED, J Protozool 1963 10 467 473 10.1111/j.1550-7408. 1963.tb01707.x 14074444
21. Intranuclear parasitism of the ciliate Euplotes by a trypanosomatid flagellate. Wille JJ, Weidner EJ, Steffens WL, J Protozool 1981 28 223 227 10.1111/j.1550-7408.1981.tb02837.x (Pubitemid 11025113)
22. Leptomonas ciliatorum n. Sp. (Kinetoplastida, Trypanosomatidae) in the macronucleus of a hypotrichous ciliate. Görtz H-D, Dieckmann J, J Protozool 1987 34 259 263 10.1111/j.1550-7408.1987.tb03171.x
23. Perkinsiella amoebae-like endosymbionts of Neoparamoeba spp., relatives of the kinetoplastid Ichthyobodo. Dyková I, Fiala I, Lukes J, Eur J Protistol 2003 52 37 52 (Pubitemid 36684418)
24. Genomic characterization of Neoparamoeba pemaquidensis (Amoebozoa) and its kinetoplastid endosymbiont. Tanifuji G, Kim E, Onodera NT, Gibeault R, Dlutek M, Cawthorn RJ, Fiala I, Lukes J, Greenwood SJ, Archibald JM, Eukaryot Cell 2011 10 1143 1146 10.1128/EC.05027-11 21666073
25. Wichterman R, The Biology of Paramecium New York: The Blakiston Company, Inc 1953 1 527
26. Bacterial endobionts of the ciliate Paramecium woodruffi. II. Endobionts of the perinuclear space. Fokin SI, Tsitologiya 1989 31 845
27. Silver impregnation of ciliated protozoa by the Chatton-Lwoff technique. Corliss JO, Stain Technol 1953 28 97 100 13056812
28. "Caedibacter macronucleorum" sp. Nov., a bacterium inhabiting the macronucleus of Paramecium duboscqui. Fokin SI, Görtz H-D, Arch Protistenkd 1993 143 319 324 10.1016/S0003-9365(11)80328-3
29. ARB: a software environment for sequence data. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, Buchner A, Lai T, Steppi S, Jobb G, Förster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, König A, Liss T, Lüssmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, et al. Nucleic Acids Res 2004 32 1363 1371 10.1093/nar/gkh293 14985472 (Pubitemid 38854737)
30. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Guindon S, Gascuel O, Syst Biol 2003 52 696 704 10.1080/10635150390235520 14530136 (Pubitemid 37365050)
31. MRBAYES: Bayesian inference of phylogenetic trees. Huelsenbeck JP, Ronquist F, Bioinformatics 2001 17 754 755 10.1093/bioinformatics/17.8.754 11524383 (Pubitemid 32851390)
32. Morphological and molecular characterization of Euplotes encysticus (Protozoa: Ciliophora: Euplotida). Fan X, Huang J, Lin X, Li J, Al-Rasheid KAS, Hu X, J Mar Biol Assoc United Kingdom 2010 90 1411 1416 10.1017/ S002531541000038X
33. New hypotrichous ciliate Euplotes encysticus sp. Nov. Yonezawa F, J Sci Hiroshima Univ Ser B, Div 1 1985 32 35 46
34. Phylogenetic studies of four species of ciliate inferred from 16S-like small subunit rRNA gene sequences. Li Y, Niu Y, Liu L, J For Res 2008 19 119 124 10.1007/s11676-008-0020-9 (Pubitemid 351950596)
35. Protozoa: Ciliophora. Bhatia BL, The fauna of British India including Ceylon and Burma, Volume I London: Taylor and Francis Ltd, Sewell RBS, 1936 1 548
36. Protozoa. 1. Free-living Protozoa. Fauna of West Bengal. Das AK, Mandal AK, Sarkar NC, Zoological Survey of India New Alipore: M-Block 1993 1 133
37. Taxonomy and ecology of ciliated Protozoa from marginal marine environments of east coast of India. Kalavati C, Raman AV, Zoological Survey of India New Alipore: M-Block 2008 1 136
38. Reconsideration of systematic relationships within the order Euplotida (Protista, Ciliophora) using new sequences of the gene coding for small-subunit rRNA and testing the use of combined data sets to construct phylogenies of the Diophrys-complex. Yi Z, Weibo S, Clamp JC, Chen Z, Gao S, Zhang Q, Mol Phylogenet Evol 2009 50 599 607 10.1016/j.ympev.2008.12.006 19121402
39. Amoebal pathogens as emerging causal agents of pneumonia. Lamoth F, Greub G, FEMS Microbiol Rev 2010 34 260 80 10.1111/j.1574-6976.2009.00207.x 20113355
40. Free-living amoebae and their intracellular pathogenic microorganisms: risks for water quality. Thomas V, McDonnell G, Denyer SP, Maillard J-Y, FEMS Microbiol Rev 2010 34 231 59 10.1111/j.1574-6976.2009.00190.x 19744244
41. Detection of a novel subspecies of Francisella noatunensis as endosymbiont of the ciliate Euplotes raikovi. Schrallhammer M, Schweikert M, Vallesi A, Verni F, Petroni G, Microb Ecol 2011 61 455 64 10.1007/s00248-010- 9772-9 21110016
42. Nuclearia pattersoni sp. N. (Filosea), a new species of amphizoic amoeba isolated from gills of roach (Rutilus rutilus), and its rickettsial endosymbiont. Dyková I, Veverková M, Fiala I, Machá cková B, Pecková H, Folia Parasitol (Praha) 2003 50 161 170 14535340 (Pubitemid 37143291)
43. "Candidatus Megaira polyxenophila" gen. Nov., sp. Nov.: Considerations on evolutionary history, host range and shift of early divergent Rickettsiae. Schrallhammer M, Ferrantini F, Vannini C, Galati S, Schweikert M, Görtz H-D, Verni F, Petroni G, PLoS One 2013 8 72581 10.1371/journal.pone. 0072581 23977321
44. A bacterium belonging to the Rickettsiaceae family inhabits the cytoplasm of the marine ciliate Diophrys appendiculata (Ciliophora, Hypotrichia). Vannini C, Petroni G, Verni F, Rosati G, Microb Ecol 2005 49 434 442 10.1007/s00248-004-0055-1 16003470 (Pubitemid 41130752)
45. Endosymbiotic bacteria in the parasitic ciliate Ichthyophthirius multifiliis. Sun HY, Noe J, Barber J, Coyne RS, Cassidy-Hanley D, Clark TG, Findly RC, Dickerson HW, Appl Env Microbiol 2009 75 7445 7452 10.1128/AEM.00850-09
46. "Candidatus Cryptoprodotis polytropus", a novel Rickettsia-like organism in the ciliated protist Pseudomicrothorax dubius (Ciliophora, Nassophorea). Ferrantini F, Fokin SI, Modeo L, Andreoli I, Dini F, Görtz H-D, Verni F, Petroni G, J Eukaryot Microbiol 2009 56 119 129 10.1111/j.1550-7408.2008.00377.x 19457052
47. Molecular identification of rickettsial endosymbionts in the non-phagotrophic volvocalean green algae. Kawafune K, Hongoh Y, Hamaji T, Nozaki H, PLoS One 2012 7 31749 10.1371/journal.pone.0031749 22363720
48. Ciliate-symbiont specificity of freshwater endosymbiotic Chlorella (Trebouxiophyceae, Chlorophyta). Summerer M, Sonntag B, Sommaruga R, J Phycol 2008 44 77 84 10.1111/j.1529-8817.2007.00455.x (Pubitemid 351225111)
49. Secondary symbiosis between Paramecium and Chlorella cells. Kodama Y, Fujishima M, In Int Rev Cell Mol Biol. Volume 2010 279 33 77
50. Endosymbiotic associations within protists. Nowack ECM, Melkonian M, Philos Trans R Soc Lond B Biol Sci 2010 365 699 712 10.1098/rstb.2009.0188 20124339
51. "Candidatus Midichloriaceae" fam. Nov. (Rickettsiales), an ecologically widespread clade of intracellular Alphaproteobacteria. Montagna M, Sassera D, Epis S, Bazzocchi C, Vannini C, Lo N, Sacchi L, Fukatsu T, Petroni G, Bandi C, Appl Entomol Zool 2013 79 3241 3248
52. "Candidatus Defluviella procrastinata" and "Candidatus Cyrtobacter zanobii", two novel ciliate endosymbionts belonging to the "Midichloria clade" Boscaro V, Petroni G, Ristori A, Verni F, Vannini C, Microb Ecol 2013 65 302 310 10.1007/s00248-012-0170-3 23296446
53. Isolation of a rickettsial pathogen from a non-hematophagous arthropod. Thepparit C, Sunyakumthorn P, Guillotte ML, Popov VL, Foil LD, Macaluso KR, PLoS One 2011 6 16396 10.1371/journal.pone.0016396 21283549