Euglenozoa: taxonomy, diversity and ecology, symbioses and viruses

Abstract

Euglenozoa is a species-rich group of protists, which have extremely diverse lifestyles and a range of features that distinguish them from other eukaryotes. They are composed of free-living and parasitic kinetoplastids, mostly free-living diplonemids, heterotrophic and photosynthetic euglenids, as well as deep-sea symbiontids. Although they form a well-supported monophyletic group, these morphologically rather distinct groups are almost never treated together in a comparative manner, as attempted here. We present an updated taxonomy, complemented by photos of representative species, with notes on diversity, distribution and biology of euglenozoans. For kinetoplastids, we propose a significantly modified taxonomy that reflects the latest findings. Finally, we summarize what is known about viruses infecting euglenozoans, as well as their relationships with ecto- and endosymbiotic bacteria.

Keywords: Diplonemida; Euglenida; Kinetoplastida; microbial eukaryotes; phylogeny; systematics.

Tree A.

Euglenozoa. A consensus tree based on multiple phylogenetic reconstructions showing relationships among major clades. The unstable position of Symbiontida is marked with a dotted line and further described in the section on euglenid taxonomy.

Plate A.

Bodonids. Light micrographs of cultured (1) Actuariola framvarensis (provided by Thorsten Stoeck); (2) Neobodo curvifilus (provided by Kristina Prokina and Denis Tikhonenkov); (3) Rhynchomonas nasuta (provided by Kristina Prokina and Denis Tikhonenkov); (4) Rhynchobodo sp. (provided by Kristina Prokina and Denis Tikhonenkov); (5) Azumiobodo hoyamushi (provided by Shinichi Kitamura and Euichi Hirose); (6) Dimastigella mimosa (provided by Kristina Prokina and Denis Tikhonenkov); (7) Bordnamonas tropicana (provided by Kristina Prokina and Denis Tikhonenkov); (8) Klosteria bodomorphis (provided by Kristina Prokina and Denis Tikhonenkov); (9) Bodo saltans (provided by Kristina Prokina and Denis Tikhonenkov); (10) Cruzella marina; (11) Allobodo chlorophagus (provided by Alastair Simpson and Yana Eglit); (12) Procryptobia sorokini (provided by Kristina Prokina and Denis Tikhonenkov); (13) Parabodo caudatus (provided by Kristina Prokina and Denis Tikhonenkov); (14) Perkinsela sp. (arrow indicates its position inside Paramoeba pemaquidensis) (provided by Ivan Fiala); (15) Giemsa-stained Trypanoplasma borreli; (16) Cryptobia vaginalis (provided by Marina N. Malysheva); (17) Toluidine-stained semi-thin section of fish gill with attached Ichthyobodo necator (provided by Iva Dyková). Scale bar, 10 µm (1–8; 10–17); 5 µm (9).

Plate B.

Trypanosoma (aquatic clade). Light micrographs of Giemsa-stained (18) T. (Trypanosoma) rotatorium ex Pelophylax kl. esculentus (provided by Klára Poloprudská); (19) T. (Trypanosoma) loricatum ex Pelophylax kl. esculentus (provided by Klára Poloprudská); (20) T. (Trypanosoma) ranarum ex Pelophylax kl. esculentus (provided by Klára Poloprudská); (21) T. (Haematomonas) clandestinus ex Caiman yacare (experimental infection) (provided by Erney Camargo and Marta Teixeira); (22) T. (Haematomonas) cf. cobitis ex Cobitis ‘taenia'; (23) T. (Haematomonas) sp. ex cichlid (provided by Iva Dyková). Scale bar, 10 µm (18–23).

Plate C.

Trypanosoma (terrestrial clade). Light micrographs of Giemsa-stained (24) T. (Trypanomorpha) avium ex Lanius collurio; (25) T. (Ornithotrypanum) everetti (provided by Gediminas Valkiūnas); (26) T. (Avitrypanum) culicavium (experimental infection) (provided by Milena Svobodová); (27) T. (Megatrypanum) theileri ex cattle (provided by Andrei Mihalca); (28) T. (Squamatrypanum) cascaveli ex Crotalus durissus (provided by Erney Camargo and Marta Teixeira); (29) T. (Crocotrypanum) terena ex Caiman yacare (provided by Erney Camargo and Marta Teixeira); (30) T. (Australotrypanum) copemani ex Bettongia penicillata (provided by Sarah Keatley and Andrew Thompson) (31) Trypanosoma livingstonei ex African bat (provided by Erney Camargo and Marta Teixeira); (32) T. (Trypanozoon) brucei brucei ex mouse (experimental infection); (33) T. (Trypanozoon) brucei equiperdum ex mouse (experimental infection); (34) T. (Trypanozoon) brucei evansi ex mouse (experimental infection); (35) T. (Herpetosoma) lewisi ex Rattus sp.; (36) T. (Aneza) vespertilionis ex Pipistrelus pipistrelus; (37) T. (Schizotrypanum) cruzi (C-shape; experimental infection); (38) T. (Schizotrypanum) cruzii (S-shape; experimental infection); (39) T. (Duttonella) vivax; (40) T. (Nannomonas) congolense. Scale bar, 10 µm (24–40).

Tree B.

Kinetoplastea. A tree summarizing multiple phylogenetic reconstructions, mostly 18S rRNA gene-based. Highlighting denotes lifestyles (see graphical legend). Asterisk denotes that the protist can be cultivated only within its host. Host Trypanosomatidae clade is collapsed (shown with a triangle) and is presented in detail on a separate figure.

Tree C.

Trypanosomatidae. A tree summarizing multiple phylogenetic reconstructions, mostly 18S rRNA gene-based. Dashed line denotes an unstable clade, which is disrupted when certain taxa are included into the analysis. For the genus Leishmania, relationships between its four subgenera are also shown. Highlighting denotes types of the life cycles (see graphical legend).

Tree D.

Trypanosoma. A tree summarizing multiple phylogenetic reconstructions, mostly 18S rRNA gene-based. All species or a selection of the most important ones (marked with three dots at the end), for which affiliation with a given subgenus and/or clade was confirmed using molecular phylogenetic methods, are listed. Highlighting denotes orders of vertebrate hosts (see graphical legend). Human parasites are underlined. Type species are shown in bold and the names accepted as senior subjective synonyms are marked with an asterisk.

Plate D.

Trypanosomatids other than Trypanosoma. Light micrographs of Giemsa-stained (41) Crithidia thermophila (culture) (42) Leptomonas seymouri (culture); (43) Lotmaria passim (culture); (44) Novymonas esmeraldas (culture); (45) Zelonia costaricensis (culture); (46) Porcisia hertigi (culture) (provided by Jovana Sádlová); (47) Endotrypanum sp. ex sloth; (48) Endotrypanum monterogeii (culture); (49) Leishmania major, metacyclic promastigote (culture) (provided by JS); (50) L. major, amastigotes in a macrophage (provided by Tereza Leštinová); (51) Herpetomonas nabiculae, promastigote (culture) (provided by Marina N. Malysheva and Alexander O. Frolov); (52) H. nabiculae, opistomastigote (provided by Marina N. Malysheva and Alaxander O. Frolov); (53) Phytomonas lipae, promastigote ex Coreus marginatus (provided by Marina N. Malysheva and Alaxander O. Frolov); (54) P. lipae, endomastigotes ex C. marginatus (provided by Marina N. Malysheva and Alaxander O. Frolov); (55) Lafontella sp. (culture); (56) Angomonas deanei (culture) (provided by Anna I. Ganyukova); (57) Kentomonas sorsogonicus (culture); (58) Strigomonas oncopelti (culture); (59) Sergeia podlipaevi (culture); (60) Jaenimonas drosophilae (culture); (61) Wallacemonas collosoma (culture); (62) Paratrypanosoma confusum (culture); (63) Blastocrithidia frustrata (culture); (64) Obscuromonas oborniki (culture); (65) Vickermania ingenoplastis (culture); (66) Blechomonas englundi (culture). Scale bar, 5 µm (41–43, 56, 57); 10 µm (44–55, 58–66).

Tree E.

Diplonemids. A tree summarizing phylogenetic reconstructions based on 18S rRNA gene. Circles denote genera with cultured representatives.

Plate E.

Diplonemids. Light micrographs of cultured (67) Diplonema papillatum; (68) Rhynchopus euleeides; (69) Sulcionema specki; (70) Artemidia motanka; (71) Eupelagonemid sp. (provided by Noriko Okamoto and Patrick Keeling); (72) Diplonema aggregatum; (73) Lacrimia lanifica; (74) Flectonema neradi; (75) Namystinia karyoxenos; (76) Hemistasia phaeocysticola. Scale bar, 10 µm (67–75).

Plate F.

Euglenids. Light micrographs of cultured (77) Cryptoglena sp. (provided by Bożena Zakryś); (78) Lepocinclis autumnalis (provided by Bozena Zakrys); (79) Phacus acuminatus (provided by Bozena Zakrys); (80) Trachelomonas armata (provided by Bozena Zakrys); (81) Monomorphina sp. (provided by Bozena Zakrys); (82) Menoidium sp. (provided by Bozena Zakrys); (83) Discoplastis spathirhyncha (provided by Bozena Zakrys); (84) Euglenaformis proxima (provided by Bozena Zakrys); (85) Euglena gracilis (provided by Bozena Zakrys); (86) Eutreptiella pomquetensis (provided by Bozena Zakrys); (87) Rapaza viridis (provided by Naoji Yubuki); (88) Jenningsia sp. (provided by Gordon Lax); (89) Peranema sp. (provided by Gordon Lax); (90) Anisonema sp. (provided by Gordon Lax); (91) Heteronema vittatum (provided by Gordon Lax); (92) Dinema sp. (provided by Gordon Lax); (93) Olkasia polycarbonata (provided by Gordon Lax); (94) Notosolenus ostium (provided by Gordon Lax); (95) Sphenomonas teres (provided by Gordon Lax); (96) Lentomonas corrugata (provided by Gordon Lax); (97) Calkinsia aureus (provided by Naoji Yubuki). Scale bar, 10 µm (77–97).

Tree F.

Euglenids and symbiontids. A tree summarizing multiple phylogenetic reconstructions, primarily based on 18S rRNA gene sequences, genes encoded by plastid genomes (Euglenophyceae), and a set of nuclear protein-coding genes retrieved from transcriptomes. Polyphyletic genera are marked with an asterisk (*). Lineages with highly unstable position are marked with a dotted line. Possible paraphyly of clades has been further described in the section on Euglenids taxonomy.