The identity and composition of the Euglenozoa

doi:10.1016/S0003-9365(97)80012-7

Archiv für Protistenkunde

Volume 148, Issue 3, October 1997, Pages 318-328

https://doi.org/10.1016/S0003-9365(97)80012-7 Get rights and content

Summary

The taxon Euglenozoa was originally created to include the kinetoplastids and euglenids only. Subsequently, euglenozoan identity and/or affinities have been suggested for Diplonema, Stephanopogon, the Hemimastigophora and several even more poorly understood eukaryotes. The Euglenozoa have only ever been defined by circumscription and/or composition; attributes that change as taxa are added or removed.

This paper seeks to refine and stabilise the concept of the Euglenozoa by redefining it as a clade identified by synapomorphy. It is proposed that the Euglenozoa be identified by the character 'heteromorphic (tubular and parallel) lattice paraxonemal rods’. Applying this definition, the Euglenozoa currently consists of four subgroups; euglenids, kinetoplastids, diplonemids (i. e. Diplonema and Rhynchopus) and Postgaardi. The reasons for the exclusion of Stephanopogon and the Hemimastigophora are also presented.

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Diplonemids are a group of flagellate protists, that belong to the phylum Euglenozoa alongside euglenids, symbiontids and kinetoplastids. They primarily inhabit marine environments, though are also found in freshwater lakes. Diplonemids have been considered as rare and unimportant eukaryotes for over a century, with only a handful of species described until recently. However, thanks to their unprecedented diversity and abundance in the world oceans, diplonemids now attract increased attention. Recent improvements in isolation and cultivation have enabled characterization of several new genera, warranting a re-examination of all available knowledge gathered so far. Here we summarize available data on diplonemids, focusing on the recent advances in the fields of diversity, ecology, genomics, metabolism, and endosymbionts. We illustrate the life stages of cultivated genera, and summarise all reported interspecies associations, which in turn suggest lifestyles of predation and parasitism. This review also includes the latest classification of diplonemids, with a taxonomic revision of the genus Diplonema. Ongoing efforts to sequence various diplonemids suggest the presence of large and complex genomes, which correlate with the metabolic versatility observed in the model species Paradiplonema papillatum. Finally, we highlight its successful transformation into one of few genetically tractable marine protists.
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Citation Excerpt :
Based on its morphological and ultrastructural features, this enigmatic marine protist has been initially considered to be a dinoflagellate (Pavillard 1922; Scherffel 1900), a euglenoid (Griessmann 1913) or, until recently, a kinetoplastid (Elbrächter et al. 1996; Senn 1911). However, a closer inspection of its ultrastructural features associated Hemistasia with another group within the phylum Euglenozoa, namely the diplonemids (Simpson 1997). Indeed, large mitochondrial cristae, a distinctive apical papilla, two parallel flagella that emerge from a deep subapical flagellar pocket, and an adjacent tubular feeding apparatus including vanes with fuzzy coats supported this inference (Elbrächter et al. 1996; Simpson and Roger 2004).
Until now, Hemistasia phaeocysticola was the only representative of the monogeneric family Hemistasiidae available in culture. Here we describe two new axenized hemistasiids isolated from Tokyo Bay, Japan. Like in other diplonemids, cellular organization of these heterotrophic protists is characterized by a distinct apical papilla, a tubular cytopharynx contiguous with a deep flagellar pocket, and a highly branched mitochondrion with lamellar cristae. Both hemistasiids also bear a prominent digestive vacuole, peripheral lacunae, and paraflagellar rods, are highly motile and exhibit diverse morphologies in culture. We argue that significant differences in molecular phylogenetics and ultrastructure between these new species and H. phaeocysticola are on the generic level. Therefore, we have established two new genera within Hemistasiidae – Artemidia gen. n. and Namystynia gen. n. to accommodate Artemidia motanka, sp. n. and Namystynia karyoxenos, sp. n., respectively. A. motanka permanently carries tubular extrusomes, while in N. karyoxenos, they are present only in starving cells. An additional remarkable feature of the latter species is the presence, in both the cytoplasm and the nucleus, of the endosymbiotic rickettsiid Candidatus Sneabacter namystus.
Phylogeny and Morphology of New Diplonemids from Japan
2018, Protist
Citation Excerpt :
They belong to Euglenozoa and are thus related to ecologically important euglenids and economically and medically relevant kinetoplastids (Adl et al. 2012; Maslov et al. 1999; Moreira et al. 2001). For a long time, diplonemids were considered a small and rare group of flagellates with only three genera and less than a dozen species formally described (Massana 2011; Simpson 1997; Vickerman 2000; von der Heyden et al. 2004). However, they emerged from obscurity thanks to molecular analysis of hundreds of planktonic samples collected across the globe by several research expeditions (de Vargas et al. 2015; Lara et al. 2009).
Diplonemids were recently found to be the most species-rich group of marine planktonic protists. Based on phylogenetic analysis of 18S rRNA gene sequences and morphological observations, we report the description of new members of the genus Rhynchopus – R. humris sp. n. and R. serpens sp. n., and the establishment of two new genera – Lacrimia gen. n. and Sulcionema gen. n., represented by L. lanifica sp. n. and S. specki sp. n., respectively. In addition, we describe the organism formerly designated as Diplonema sp. 2 (ATCC 50224) as Flectonema neradi gen. n., sp. n. The newly described diplonemids share a common set of traits. Cells are sac-like but variable in shape and size, highly metabolic, and surrounded by a naked cell membrane, which is supported by a tightly packed corset of microtubules. They carry a single highly reticulated peripheral mitochondrion containing a large amount of mitochondrial DNA, with lamellar cristae. The cytopharyngeal complex and flagellar pocket are contiguous and have separate openings. Two parallel flagella are inserted sub-apically into a pronounced flagellar pocket. Rhynchopus species have their flagella concealed in trophic stages and fully developed in swimming stages, while they permanently protrude in all other known diplonemid species.
Euglenoid pellicle morphogenesis and evolution in light of comparative ultrastructure and trypanosomatid biology: Semi-conservative microtubule/strip duplication, strip shaping and transformation
2017, European Journal of Protistology
Uniquely in eukaryotes, euglenoid pellicles comprise longitudinal proteinaceous, epiplasmic strips underlain by microtubules. Contradictory interpretations of pellicle microtubule duplication and segregation assumed opposite microtubule polarity from kinetoplastid Euglenozoa and conservative microtubule segregation. Distigma shows new pellicle microtubules nucleating posteriorly as in trypanosomatids, unifying euglenoid and kinetoplastid pellicle morphogenesis, but strip-growth is unpolarised. Epiplasmic insertion and cutting make new strip junctions between alternating wide and narrow daughter strips that grow intussusceptively. Nanotubules, overlooked epiplasm-associated components, define strip edges. At strip heel/toe junctions all euglenoids have a morphogenetic centre microtubule mt2/3 pair. Arguably, proteolysis, epiplasmic growth, and toe-nanotubule-associated epiplasmic scission initiate daughter strips, separating old mts2/3; new mt2/3/bridge-B assembly, sub-heel scission, nanotubule-bridge-A assembly complete duplication. Only mt2/3 pair fully enters the canal, one master microtubule also the reservoir, other pellicle microtubules terminating near canal rims. A related cytokinesis model involving ciliary attachment zone duplication explains near-universally even spirocute strip number. I consider Serpenomonas and Entosiphon alternating heteromorphic strips developmental stages of ‘strip transformation’; explain intergroup diversity of strip morphology and dorsoventral strip differentiation causally by specific pellicle-complex components; propose centrin-based mechanisms for strip shaping and euglenoid movement; unify pellicle cytokinetic microtubule segregation across Euglenozoa; and discuss origin and diversification of pellicle complexes.
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Citation Excerpt :
Looking at their closest kins, represented by “classic” diplonemids, Hemistasia and the kinetoplastid flagellates, does not provide useful hints because those groups evolved a wide array of life strategies ranging from feeding on bacteria, predation, to parasitism and/or obligate symbiosis [7, 9, 25, 26]. The extreme species richness of the DSPD I diplonemids could stem from their diverse trophic interactions, ranging from bacterivory or parasitism, as seen in related kinetoplastids [7, 24], eukaryovory characteristic for the sister-branching Hemistasia [9], or even the so-far-overlooked grazing on viruses [27–30]. Recent results suggest that many species-rich planktonic groups (e.g., within the dinozoans and metazoans) are predominantly parasites [6].
The world’s oceans represent by far the largest biome, with great importance for the global ecosystem [1, 2, 3, 4]. The vast majority of ocean biomass and biodiversity is composed of microscopic plankton. Recent results from the Tara Oceans metabarcoding study revealed that a significant part of the plankton in the upper sunlit layer of the ocean is represented by an understudied group of heterotrophic excavate flagellates called diplonemids [5, 6]. We have analyzed the diversity and distribution patterns of diplonemid populations on the extended set of Tara Oceans V9 18S rDNA metabarcodes amplified from 850 size- fractionated plankton communities sampled across 123 globally distributed locations, for the first time also including samples from the mesopelagic zone, which spans the depth from about 200 to 1,000 meters. Diplonemids separate into four major clades, with the vast majority falling into the deep-sea pelagic diplonemid clade. Remarkably, diversity of this clade inferred from metabarcoding data surpasses even that of dinoflagellates, metazoans, and rhizarians, qualifying diplonemids as possibly the most diverse group of marine planktonic eukaryotes. Diplonemids display strong vertical separation between the photic and mesopelagic layers, with the majority of their relative abundance and diversity occurring in deeper waters. Globally, diplonemids display no apparent biogeographic structuring, with a few hyperabundant cosmopolitan operational taxonomic units (OTUs) dominating their communities. Our results suggest that the planktonic diplonemids are among the key heterotrophic players in the largest ecosystem of our biosphere, yet their roles in this ecosystem remain unknown.
Higher classification and phylogeny of Euglenozoa
2016, European Journal of Protistology
Discoveries of numerous new taxa and advances in ultrastructure and sequence phylogeny (including here the first site-heterogeneous 18S rDNA trees) require major improvements to euglenozoan higher-level taxonomy. I therefore divide Euglenozoa into three subphyla of substantially different body plans: Euglenoida with pellicular strips; anaerobic Postgaardia (class Postgaardea) dependent on surface bacteria and with uniquely modified feeding apparatuses; and new subphylum Glycomonada characterised by glycosomes (Kinetoplastea, Diplonemea). Euglenoida comprise two new infraphyla: Entosiphona with three feeding rods and Dipilida ancestrally with two. Dipilida comprise basal superclass Rigimonada with longitudinal rigid strips [i.e. new classes Stavomonadea (Petalomonadida, Decastavida and new order Heterostavida) and Ploeotarea (Ploeotiida) with contrasting oral cytoskeletons] and derived superclass Spirocuta with more numerous spirally arranged, often slideable, strips (clade Peranemea/Euglenophyceae) and a different, highly conserved microtubule pattern at strip joints. Peranemea comprise four orders: Peranemida (anterior gliding, protrusible rods), and three new, Anisonemida (posterior gliders), Natomonadida (swimmers including phagotrophic new suborder Metanemina and osmotrophic suborder Rhabdomonadina), and Acroglissida (anterior gliders with cytoproct). I establish orders Entosiphonida, Rapazida, Bihospitida; and seven new euglenoid families (Entosiphonidae, peranemean Neometanemidae, Rapazidae, two stavomonad, two ploeotiid) and three new postgaardian, and three kinetoplastid families (Neobodonidae, Rhynchomonadidae, Parabodonidae), plus new diplonemid family Hemistasiidae for Hemistasia.

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¹: Author’s address: Alastair G. B. Simpson, School of Biological Sciences, Building A08, University of Sydney, 2006, Australia; Ph. 61 2 9351 3536; Fax 61 2 9351 4119

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The identity and composition of the Euglenozoa

Summary

Biol. Cell

BioSystems

BioSystems

Arch. Protistenkd.

Arch. Protistenkd.

BioSystems

Europ. J. Protistol.

Biol. Cell

Int. Rev. Cytol.

BioSystems

Europ. J. Protistol.

Europ. J. Protistol.

Europ. J. Protistol.

Europ. J. Protistol.

Arch. Protistenkd.

Arch. Protistenkd.

BioSystems

Europ. J. Protistol.

Europ. J. Protistol.

Arch. Protistenkd.

Terminology and nomenclature of the cytoskeletal elements associated with the flagellar/ciliary apparatus in protists

Protoplasma

Ultrastructure and 18S rRNA gene sequence for Pelagomonas calceolata gen. et sp. nov. and the description of a new algal class, the Pelagophyceae classis nov

J. Phycol.

Monophyly and associated terms

Syst. Zool.

Des trichocystes chez les bodonidés, un caractère phylogénétique supplémentaire entre Kinetoplastida et Euglenida

Protistologica

Comparison et évolution des structures cellulaires chez plusieurs espèces de bodonidés et cryptobiidés appartenant aux genres Bodo, Cryptobia et Trypanoplasma (Kinetoplastida, Mastigophora)

Protistologica

The origin of eukaryote and archaebacterial cells

Ann. N. Y. Acad. Sci.

Zooflagellate phylogeny and classification

Cytology

Taxonomic characterization of the suprafamilial groups in a revision of recently proposed schemes of classification for the phylum Ciliophora

Trans. Amer. Micros. Soc.

The kingdoms of organisms — from a microscopist's point of view

Trans. Am. Microsc. Soc.

An interim utilitarian (“user-friendly”) hierarchical classification and characterization of the protists

Acta Protozool.

Structural characterization of Eutreptia (Euglenophyta). III. Flagellar structure and possible function of the paraxonemal rods

Phycologia

Evolutionary trends in euglenoids

Arch. Protistenkd.

An ultrastructural study of Lentomonas applanatum (Preisig) N. G. (Euglenida)

J. Euk. Microbiol.

Microbial diversity and activity in a Danish fjord with anoxic deep water

Ophelia

Percolomonas cosmopolitus (Ruinen) n. gen., a new type of filter feeding flagellate from marine plankton

J. Mar. Biol. Ass. U. K.

Revision of the family Spironemidae Doflein (Protista, Hemimastigophora), with description of two new species, Spironema terricola n. sp. and Stereonema geiseri, n. g., n. sp

J. Euk. Microbiol.

Über marine Flagellaten

Arch. Protistenkd.