Josef Juráň^1,2

¹University of South Bohemia in České Budějovice (České Budějovice, Czech Republic)

²Třeboň Experimental Garden and Gene Pool Collections, Institute of Botany of the CAS
(Třeboň, Czech Republic)

УДК 582.277

Фотосинтезирующие эвглениды представляют собой обширную группу жгутиковых, обладающих широкой морфологической изменчивостью, которые встречаются в большинстве пресноводных, морских и солоноватых местообитаниях, а также в экстремальных условиях с низким pH или во влажной почве. В настоящей работе приводится краткое обобщение возможных причин морфологической изменчивости эвгленовых водорослей (влияние факторов окружающей среды, фенотипическая пластичность в процессе онтогенеза), а также современные представления о таксономии этих протистов.

Ключевые слова: фотосинтезирующие эвглениды; таксономия; филогения; экология; биогеография

Photosynthetic euglenoids represent a large group of flagellates, which could be found in most freshwater, marine and brackish habitats, but also in extreme environments with low pH or in moist soil. The existence of this group has been known for a relatively long led to the description of wide morphological variability. In my contribution, I briefly summarize the possible causes of this morphological variability (effect of the environment and phenotypic plasticity during ontogenesis) and current knowledge about the taxonomy of these protist organisms, showing the most recent changes and descriptions of new genera.

Ключевые слова: photosynthetic euglenoids; taxonomy; phylogeny; ecology; biogeography

Euglenoids form a diverse group of eukaryotic organisms that may have arisen a billion years ago and it is probably one of the oldest eukaryotic lineages. They are commonly unicellular free-living flagellates (except the genus Colacium forming sessile colonies). The main part of photosynthetic euglenoids live in freshwater and only some species occur in brackish water or in seas and oceans.  Photosynthetic euglenoids can  be presented to varying degrees in all types of freshwater habitats, often also in extreme, e.g. post-harvest areas with significantly low pH (Triemer, Zakryś, 2015). Their research has a relatively long tradition – the first description of the photosynthetic euglenoids was made by Ehrenberg at the beginning of the 19th century – Euglena (Ehrenberg, 1830), Cryptoglena (Ehrenberg, 1832), Colacium (Ehrenberg, 1834) and Trachelomonas (Ehrenberg, 1834). During the 19th century, other traditional genera were described – Phacus (Dujardin, 1841), Lepocinclis (Perty, 1849), Monomorphina (Mereschkowsky, 1877) and Ascoglena (Stein, 1878), the last traditional genus Strombomonas was described at the beginning of the 20^th century by Deflandre (1930). Studies of euglenoids, as well as other algal or protistian groups, were based on morphological features, which were the key factor of the taxonomic studies of euglenoids during the whole 19th and most of the 20^th century. During that relatively long research period, a huge number of species and intraspecific taxa in these listed genera were described. According to the AlgaeBase (Guiry, Guiry, 2021), a common-used source about algal diversity and taxonomy, there was 1580 species described in thirteen genera currently described from which about 60 % have been flagged as accepted taxonomically, on the intraspecific level 2000 taxa are in the database listed. Especially in some genera (e.g. Euglena or Trachelomonas) there is significant phenotypic variability, both at the species and especially at the intraspecific level. With this variability, the question “What causes this variability?” arises.

The huge morphological variability could be probably explained by using two main factors: (1) the impact of environmental conditions to the euglenoid morphology and (2) the role of the ontogeny stage in which species is observed. Several studies support the theory of the environmental impact on the euglenoid morphology. Conforti (1998), Conforti et al. (2017) and Nannavecchia et al. (2014) studied morphological changes of several euglenoids in response to the organic enrichment of laboratory cultures of these algae. Results show cell deformation, the extraordinary accumulation of paramylon grains and the development of larger paramylon grains in higher frequency than which is typical for euglenoids from enriched cultures. Moreover, similar results have been shown in studies with cultures on a natural condition, e.g. Bauer et al. (2012) designed bioassay based on Lepocinclis acus cultures in the semipermeable microcosm as model organisms in order to study the impact of the chemical and textile industry on the environment of river in Argentina. Their results, again, show significant increase in the cellular volume for species together with abnormal shape in the studied sites. Second important factor which could explain a huge number of described species and infraspecific taxa is the variability of euglenoids during their ontogeny. The morphological variability of the several species of the genus Trachelomonas was studied by Pringsheim (1953) and Singh (1956a,b). Their results show that the Trachelomonas species studied in the clonal cultures exhibit a morphological variability on their monads as well as their loricae during the life cycle. Authors conclude that this variability is a rather complicating factor in describing new species from natural populations, because descriptions of new taxa were based on few individuals from the population without deeper study of their life cycle at all. Owing to the modern research, the role of ontogeny is well documented in the work focused on the common euglenoid species Monomorphina pyrum by Kosmala et al. (2007b), who provided a revision of M. pyrum and morphologically similar taxa using a morphological-molecular approach and one of the results was synonymization of several Monomorphina taxa with M. pyrum. Authors support their results by detailed discussion about reasons why such a high number of morphologically similar organisms were described by different authors as separate species. The description of these species was based on differences from the “typical” M. pyrum, e.g. the presence of two chloroplasts, the absence of large paramylon grains, and the degree of cell flatness. Authors connect this description with the observation of M. pyrum in different stages of its life cycles and support this claim with a detailed description of changes in M. pyrum during ontogeny. The second study connected with the variability of euglenoids during their ontogeny is the study of natural populations of the common Trachelomonas caudata species (Wołowski, et al., 2016). Authors used basic morphometrical data in the combination with the literature sources to compare T. caudata with morphologically similar taxa (T. caudata f. pseudocaudata, T. fusiformis, T. allorgei, T. mollesta and T. bernardinensis) – as a result of this comparison, authors claim that all studied species should be synonymized with the T. caudata. According to this study, we could assume that the description of these species was connected with the observed stage of T. caudata life cycle as was shown in the previous study about Monomorpina pyrum.

Euglenoids, as well as another algal and protistian group, have a global distribution pattern. Notwithstanding, there are several questions connected with the euglenoids’ distribution on the species level – the existence of worldwide distributed species and, on the other hand, there are theories about endemic species. With these tasks, two main distributional theories about microorganisms are connected – ubiquity theory, postulating that protists are practically ubiquitous, mainly due to their small size (Finlay et al., 1996, 2004; Finlay, Fenchel 2004; Fenchel, Finlay, 2004) and the theory of moderate endemism, arguing that some protist organisms have a global ubiquitous distribution, but some have a limited geography and they could may be considered endemic (Foissner, 1999, 2006, 2007). There are several algal groups, e.g. diatoms, silica-scaled chrysophytes and desmids – with well-studied biogeography, e.g. comprehensive studies of (e.g. Kristiansen, 1996; Foissner, Hawksworth, 2009; Fontaneto, 2011). Concerning other algal groups, there are still present some gaps and their biogeography is still a challenging task. Similarly, this is the case of euglenoids, too. The detailed discussion on biogeography of the euglenoids took place in the work based on finding a species of Trachelomonas saccasii, described from Africa, in the European mesotrophic pond (Juráň, Couté, 2018) – finding of this species highlights current knowledge gaps regarding the biogeography and worldwide distribution of euglenoids. Authors propose several euglenoid species with well-defined morphology and with a limited geographical distribution (Colacium epiphyticum, C. minimum, Lepocinclis crassicollis, Phacus plicatus, Trachelomonas argentinensis, T. hemispherica and T. magdaleniana) as potential flagship species for the better understanding of the euglenoids biogeography. There are several important questions in the study of the biogeography of photosynthethic euglenoids: (1) How much is our knowledge of the global biogeography of euglenoids affected by the undersampling effect? (2) Can we draw conclusions about global distribution of euglenoids if the taxonomic situation of many species is not fully resolved? (3) Are there endemic species of euglenoids? (4) Are globally widespread species really genetically the same species, or does cryptic diversity play a role here?

In the past, several authors tried to solve some problems of the euglenoid taxonomy caused by the morphological variability mentioned above and several revisions were published. The predominance of these revisions is based primarily on morphologically based studies, which were later supplemented by some ultrastructural data based on cytochemical staining and ultrastructure. Despite the large number of taxonomic works, the situation in the taxonomy of euglenophytes was still not satisfactorily solved in many cases. The solution to these taxonomic problems came with methods of molecular phylogenetics at the turn of the 20^th and the 21^st centuries. Zakryś et al. (2002) resolved problem of Euglena geniculata and E. myxocylindracea, which are according to authors‘ results genetically and morphologically identical; Marin et al. (2003) studied euglenoids phylogeny based on SSU rDNA sequences, authors renewed the genus Monomorphina, which was a sub-part of the genus Phacus and made changes in the taxonomic position of common worldwide members of the genus Euglena (E. acus, E. oxyuris, E. spirogyra, E. tripteris) to the genus Lepocinclis; Shin & Triemer (2004) focused on a type of species of the genus Euglena – E. viridis; Zakryś et al. (2004) studied isolates of the common Euglena agilis using combination of ITS2 of extrachromosomal rDNA and the chloroplast SSU rDNA sequences. During the last ten years, several revisions were made in the number of euglenoid genera, e.g. Euglena sensu lato (Bennet et al., 2014; Karnkowska-Ishikawa et al., 2011, 2012, 2013; Kosmala et al., 2009; Linton et al., 2010; Łukomska‐Kowalczyk et al., 2020b; Triemer et al., 2006), Lepocinclis (Kosmala et al., 2005; Łukomska‐Kowalczyk et al., 2020a), Monomorphina (Kosmala et al., 2007b; Nudelman et al., 2005) and Phacus (Karnkowska-Ishikawa, et al., 2010; Kosmala et al., 2007a; Łukomska-Kowalczyk et al., 2015). The question about cryptic species diversity is studied and discussed in several works, Kim et al. (2013a, b) described quite a high number of cryptic species in the genus Monomorphina and Cryptoglena; Kim & Shin (2014) studied the cryptic diversity in the genus Phacus with the description of seven new species and the work about morphological and genetic diversity of Euglena deses group with an emphasis on cryptic species was published by Kim et al. (2016).

The results of modern molecular data-based studies show that “classical” genera whose taxonomy was and still is partly based on morphology are complex of morphologically similar genera. This phenomenon is very well demonstrated by the situation in the genus Euglena in the morphology-based concept. Some representatives of the Euglena were reclassified into existing genera, e.g. Lepocinclis (former members of the Rigidiae section ⟶ Lepocinclis acus, L. fusca, L. oxyuris, L. tripteris, L. spirogyroides, Marin et al., 2003) or Phacus (Euglena limnophila ⟶ P. limnopilus, Linton et al., 2010). In the case of some Euglena-like representatives, these turned out to be completely new lineages and were described as new genera, e.g. Discoplastis (Euglena spathirhyncha, E. adunca ⟶ D. spathirhyncha, D. adunca, Triemer et al., 2006), Euglenaria (Euglena anabaena, E. caudata, E. clavata ⟶ Euglenaria anabaena, E. caudata, E. clavata, Linton et al., 2010), Euglenaformis (Euglena proxima ⟶ Euglenaformis proxima, Bennett et al., 2014)  and Flexiglena (Euglena variabilis ⟶ Flexiglena variabilis, Łukomska-Kowalczyk et al., 2020b). In the future, due to significant morphological variability, further changes and shifts can be expected within the genus Euglena, but also in many other genera, such as the genus Trachelomonas, whose morphological variability is comparable if not greater than that of the genus Euglena.

The effort to understand the taxonomy and phylogenetic relationships of euglenoids also brings new methods. Bennet & Triemer (2012) designed new methods for obtaining nuclear gene sequences from filed samples. Authors use this method successfully in the study of position of Lepocinclis horridus (formerly Phacus horridus) and Lepocinclis helicoideus (formerly Euglena helicoideus). This method could solve the problem with the complicated or impossible cultivation of some species and the inability to work with cultures of these organisms. Łukomska-Kowalczyk et al. (2016) and Gumińska et al. (2021) focused on the use of barcoding in the photosynthetic euglenoids and, as a result of their studies, authors suggested two molecular markers (COI and 18S rDNA) as potential DNA barcodes. Despite a significant progress in this area, there is still a relatively high number of species complexes together with some genera, e.g. Colacium, Strombomonas and Trachelomonas, where molecular data is insufficient or fully missing. For future understanding of the diversity and biogeography of photosynthetic euglenoids, it is necessary to use in their detailed study both local (regional) and global scales. The most effective tool in this situation is the use of the so-called polyphasic approach, which combines data on morphology, ultrastructure, molecular biology and also ecological data – these problems bring tasks and challenges for further researches.

The author declares no conflicts of interest.

Автор заявляет об отсутствии конфликта интересов, требующего раскрытия в данной статье.

Список литературы

1. Bauer D.E., Conforti V., Ruiz L., Gomez N. An in situ test to explore the responses of Scenedesmus acutus and Lepocinclis acus as indicators of the changes in water quality in lowland streams // Ecotoxicology and Environmental Safety. 2012. V. 77. P. 71–78. DOI: https://doi.org/10.1016/j.ecoenv.2011.10.021
2. Bennett M. S., Triemer R.E. A new method for obtaining nuclear gene sequences from field samples and taxonomic revisions of the photosynthetic euglenoids Lepocinclis (Euglena) helicoideus and Lepocinclis (Phacus) horridus (Euglenophyta) // Journal of Phycology. 2012. V. 48. P. 254–260. DOI: https://doi.org/10.1111/j.1529-8817.2011.01101.x
3. Bennett, M.S., Wiegert, K.E., Triemer R.E. Characterization of Euglenaformis gen. nov. and the chloroplast genome of Euglenaformis [Euglena] proxima (Euglenophyta) // Phycologia. 2014. V. 53. P. 66–73. DOI: https://doi.org/10.2216/13-198.1
4. Conforti V. Morphological changes of Euglenophyta in response of organic enrichment // Hydrobiologia. 1998. V.369. P. 277–285. DOI: https://doi.org/10.1023/A:1017049910481
5. Conforti V., Ruiz L.B., Leonardi P.I. Ultrastructural Alterations in Lepocinclis acus (Euglenophyta) Induced by Medium with High Organic Matter Content // Frontiers in Ecology and Evolution. 2017. V. 5. P. 141. DOI: https://doi.org/10.3389/fevo.2017.00141
6. Deflandre G. Strombomonas nouveau genere d'euglénacées (Trachelomonas Ehr. pro parte) // Archiv für Protistenkunde 1930 V. 69. P. 551–614.
7. Dujardin F. Histoire naturelle des Zoophytes, Infusoires, comprenant la physiologie et la clasification de ces animaux et la manière de les étudier à l'aide du microscope. – Paris: Librarie Encyclopédique de Roret, 1841. – 684 p.
8. Ehrenberg C.G. Neue Beobachtungen über blutartige Erscheinungen in Aegypten, Arabien und Sibirien, nebst einer Uebersicht und Kritik der früher bekannten // Annalen der Physik und Chemie, Ser. 2 1830. V. 8. P. 477–514.
9. Ehrenberg C.G. Über die Entwickelung und Lebensdauer der Infusionsthiere; nebst ferneren Beiträgen zu einer Vergleichung ihrer organischen Systeme // Abhandlungen der Königlichen Akademie Wissenschaften zu Berlin, Physikalische Klasse. 1832. P. 1–154.
10. Ehrenberg C.G. Dritter Beitrag zur Erkenntniss grosser Organisation in der Richtung des kleinsten Raumes // Abhandlungen der Königlichen Akademie der Wissenschaften zu Berlin. 1834. P.145–336.
11. Mereschkowsky K.S. Etjudy nad prostejsimi zivotnymi severa Rossii // Trudy Sankt-Peterburgskago Obshchestva Estestvoisptatele 1877 V. 8. P. 1–299.
12. Fenchel T., Finlay B.J. The ubiquity of small species: patterns of local and global diversity // BioScience 2004. V. 54. P. 777–784. DOI: https://doi.org/10.1641/0006-3568(2004)054[0777:TUOSSP]2.0.CO;2
13. Finlay B.J., Corliss J.O., Esteban G., Fenchel T. Biodiversity at the Microbial Level: The Number of Free-Living Ciliates in the Biosphere // The Quarterly Review of Biology. 1996. V.71. P. 221–237. DOI: https://doi.org/10.1086/419370
14. Finlay B.J., Esteban G.F., Fenchel T. Protist Diversity is Different? // Protist. 2004. V. 155. P. 15–22. https://doi.org/10.1078/1434461000160
15. Finlay B.J., Fenchel T. Cosmopolitan metapopulations of free-living microbial eukaryotes // Protist. 2004. V. 155. P. 237–244. DOI: https://doi.org/10.1078/143446104774199619
16. Foissner W. Protist Diversity: Estimates of the Near-Imponderable // Protist. 1999. V. 150. P. 363–368. DOI: https://doi.org/10.1016/S1434-4610(99)70037-4
17. Foissner W. Biogeography and Dispersal of Micro-organisms: A Review Emphasizing Protists // Acta Protozoologica. 2006. V. 45. P. 111–136.
18. Foissner W. Dispersal and Biogeography of Protists: Recent Advances // Japanese Journal of Protozoology 2007. V. 40. P. 1–16. DOI: https://doi.org/10.18980/jjprotozool.40.1_1
19. Foissner W., Hawksworth D.L. Protist Diversity and Geographical Distribution. – Dordrecht: Springer, 2009. – 209 p.
20. Fontaneto D. Biogeography of Microscopic Organisms. Is Everything Small Everywhere? – New York: Cambridge University Press, 2011. – 365 p.
21. Gumińska N., Łukomska‐Kowalczyk M., Chaber K., Zakryś B., Milanowski R. Evaluation of V2 18S rDNA barcode marker and assessment of sample collection and DNA extraction methods for metabarcoding of autotrophic euglenids // Environmental Microbiology. 2021. DOI: https://doi.org/10.1111/1462-2920.15495
22. Guiry M.D., Guiry G.M. AlgaeBase. 2021. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org (date: 15.07.2021).
23. Juráň J., Couté A. African Trachelomonas saccasii found in a European mesotrophic pond (Czech Republic). Implication for euglenoid biogeography and recommendations for euglenoid flagship species // Phytotaxa. 2018. V. 334. P. 201–214. DOI: https://doi.org/10.11646/phytotaxa.334.3.1
24. Karnkowska-Ishikawa A., Milanowski R., Triemer R.E., Zakryś B. Taxonomic revisions of morphologically similar species from two genera: Euglena (E. granulata and E. velata) and Euglenaria (Eu. anabaena, Eu. caudata, Eu. clavata) // Journal of Phycology. 2012. V. 48. P. 729–739. DOI: https://doi.org/10.1111/j.1529-8817.2012.01140.x
25. Karnkowska-Ishikawa A., Milanowski R., Triemer R. E., Zakryś B. A redescription of morphologically similar species from the genus Euglena: E. laciniata, E. sanguinea, E. sociabilis and E. splendens // Journal of Phycology. 2013. V. 49. P. 616–626. DOI: https://doi.org/10.1111/jpy.12072
26. Karnkowska-Ishikawa A., Milanowski R., Zakryś B. The species Euglena deses revisited: New morphological and molecular data // Journal of Phycology. 2011. V. 47. P. 653–661. DOI: https://doi.org/10.1111/j.1529-8817.2011.00982.x
27. Karnkowska‐Ishikawa A., Milanowski R., Kwiatowski J., Zakryś B. Taxonomy of the Phacus oscillans (Euglenaceae) and Its Close Relatives-Balancing Morphological and Molecular Features // Journal of Phycology. 2010. V.46. P. 172-182. DOI: https://doi.org/10.1111/j.1529-8817.2009.00765.x
28. Kim J.I., Linton E.W., Shin W. Morphological and genetic diversity of Euglena deses group (Euglenophyceae) with emphasis on cryptic species // Algae. 2016. V. 31. P. 219–230. DOI: https://doi.org/10.4490/algae.2016.31.9.9
29. Kim J.I., Shin W. Molecular phylogeny and cryptic diversity of the genus Phacus (Phacaceae, Euglenophyceae) and the descriptions of seven new species // Journal of Phycology. 2014. V. 50. P. 948–959. DOI: https://doi.org/10.1111/jpy.12227
30. Kim J.I., Shin W., Triemer R.E. Phylogenetic reappraisal of the genus Monomorphina (Euglenophyceae) based on molecular and morphological data // Journal of Phycology. 2013a. V. 49. P. 82–91. DOI: https://doi.org/10.1111/jpy.12018
31. Kim J.I., Shin W., Triemer R.E. Cryptic speciation in the genus Cryptoglena (Euglenaceae) revealed by nuclear and plastid SSU and LSU rRNA gene // Journal of Phycology. 2013b. V. 49. P. 92–102. DOI: https://doi.org/10.1111/jpy.12032
32. Kosmala S., Karnkowska A., Milanowski R., Kwiatowski J., Zakryś B. The phylogenetic and taxonomic position of Lepocinclis fusca comb. nova (=Euglena fusca) (Euglenaceae). Morphological and molecular justification // Journal of Phycology. 2005. V. 41. P. 258–267. DOI: https://doi.org/10.1111/j.1529-8817.2005.00141.x
33. Kosmala S., Karnkowska-Ishikawa A., Milanowski R., Kwiatowski J., Zakryś B. Phylogeny and systematics of species from the genus Euglena (Euglenaceae) with axial, stellate chloroplasts based on morphological and molecular data – New taxa, emended diagnoses and epitypifications // Journal of Phycology. 2009. V. 45. P. 464–481. DOI: https://doi.org/10.1111/j.1529-8817.2009.00653.x
34. Kosmala S., Bereza M., Milanowski R., Kwiatowski J., Zakryś B. Morphological and molecular examination of relationships and epitype establishment of Phacus pleuronectes, Phacus orbicularis and Phacus hamelii // Journal of Phycology. 2007a. V. 43. P.1071–1082. DOI: https://doi.org/10.1111/j.1529-8817.2007.00386.x
35. Kosmala S., Milanowski R., Brzóska K., Pękal, M., Kwiatowski J., Zakryś B. Phylogeny and systematics of the genus Monomorphina (Euglenaceae) based on morphological and molecular data // Journal of Phycology. 2007b. V. 43. P.171–185. DOI: https://doi.org/10.1111/j.1529-8817.2006.00298.x
36. Kristiansen J. Biogeography of freshwater algae. – Dordrecht: Kluwer, 1996. – 161 p.
37. Linton E.W., Karnkowska-Ishikawa A., Kim J.I., Shin W., Bennett M., Kwiatowski J., Zakryś B., Triemer R. E. Reconstructing euglenoid evolutionary relationships using three genes: Nuclear SSU and LSU, and chloroplast 16S rDNA sequences and the description of Euglenaria gen. nov. (Euglenophyta) // Protist. 2010. V. 161. P. 603–619. DOI: https://doi.org/10.1016/j.protis.2010.02.002
38. Łukomska‐Kowalczyk M., Chaber K., Fells A., Milanowski R., Zakryś B. Molecular and morphological delimitation of species in the group of Lepocinclis ovum‐like taxa (Euglenida) // Journal of phycology. 2020a. V. 56. P. 283–299. DOI: https://doi.org/10.1111/jpy.12949
39. Łukomska‐Kowalczyk M., Chaber K., Fells A., Milanowski R., Zakryś B. Description of Flexiglena gen. nov. and new members of Discoplastis and Euglenaformis (Euglenida) // Journal of Phycology. 2020b. DOI: https://doi.org/10.1111/jpy.13107
40. Łukomska‐Kowalczyk M., Karnkowska A., Krupska M., Milanowski R., Zakryś B. DNA barcoding in autotrophic euglenids: evaluation of COI and 18S rDNA // Journal of Phycology. 2016. V. 52. P. 951–960. DOI: https://doi.org/10.1111/jpy.12439
41. Łukomska-Kowalczyk M., Karnkowska A., Milanowski R., Łach Ł., Zakryś B. Delimiting species in the Phacus longicauda complex (Euglenida) through morphological and molecular analyses // Journal of Phycology. 2015. V. 51. P. 1147–1157. DOI: https://doi.org/10.1111/jpy.12352
42. Marin B., Palm A., Klingberg M., Melkonian M. Phylogeny and taxonomic revision of plastid-containing euglenophytes based on SSU rDNA sequence comparisons and synapomorphic signatures in the SSU rRNA secondary structure // Protist. 2003. V. 154. P. 99–145. DOI: https://doi.org/10.1078/143446103764928521
43. Nannavecchia P., Tolivia A., Conforti V. Ultrastructural alterations in Phacus brachykentron (Euglenophyta) due to excess of organic matter in the culture medium // Ecotoxicology and Environmental Safety. 2014. V. 101. P. 36–41. DOI: https://doi.org/10.1016/j.ecoenv.2013.12.007
44. Nudelman M.A., Leonardi P.I., Conforti V., Farmer M.A., Triemer R.E. Fine structure and taxonomy of Monomorphina aenigmatica comb. nov (Euglenophyta) // Journal of Phycology. 2005. V. 42. P.194–202. DOI: https://doi.org/10.1111/j.1529-8817.2006.00170.x
45. Perty M. Über verticale Verbreitung mikroskopischer Lebensformen // Mittheilungen der Naturforschenden Gesellschaft in Bern. 1849. P. 17–45.
46. Pringsheim E.G. Observation on Some Species of Trachelomonas Grown in Culture // New Phytologist. 1953. V. 52. P. 93–113, 238–266.
47. Shin W., Triemer R.E. Phylogenetic analysis of the genus Euglena (Euglenophyceae) with the particular reference to the type species Euglena viridis // Journal of Phycology 2004. V. 40. P. 758–771. DOI: https://doi.org/10.1111/j.1529-8817.2004.03142.x
48. Singh K.P. Studies in the genus Trachelomonas. I. Description of six organisms in cultivation // American Journal of Botany. 1956a. V. 43. P. 258–266.
49. Singh K.P. Studies in the genus Trachelomonas. II. Cell structure and reproduction with special reference to T. grandis // American Journal of Botany. 1956b. V. 43. P. 274–280.
50. Triemer R.E., Linton E., Shin W., Nudelman A., Monfils A., Bennett M., Brosnan S. Phylogeny of the euglenales based upon combined SSU and LSU rDNA sequence comparisons and desciption of Discoplastis gen. nov. (Euglenophyta) // Journal of Phycology. 2006. V. 42. P. 731–740. DOI: https://doi.org/10.1111/j.1529-8817.2006.00219.x
51. Triemer R. E., Zakryś B. Photosynthetic euglenoids / Wehr J.D., Sheath, R.G., Kociolek, J.P. (eds.). Freshwater Algae of North America Amsterdam: Elsevier, 2015. P. 459–483.
52. Stein F. Der Organismus der Infusionsthiere nach eigenen forschungen in systematischere Reihenfolge bearbeitet. III. Abtheilung. Die Naturgeschichte der Flagellaten oder Geisselinfusorien. I. Hälfte, Den noch nicht abgeschlossenen allgemeinen Theil nebst erklärung: Der sämmtlichen Abbildungen enthaltend. Leipzig: Verlag von Wilhelm Engelmann, 1878. 154 p.
53. Wołowski K., Poniewozik M., Juráň J. Morphological variability of loricae in Trachelomonas caudata complex (Euglenophyta) // Cryptogamie, Algologie. 2016. V. 37. P. 97–108. DOI: https://doi.org/10.7872/crya/v37.iss2.2016.97
54. Zakryś B., Empel J., Milanowski R., Gromadka R., Borsuk P., Kedzior M., Kwiatowski J. Genetic variability of Euglena agilis (Euglenophyceae) // Acta Societaits Botanicorum Poloniae 2004. V. 73. P. 305–309. DOI: https://doi.org/10.5586/asbp.2004.039
55. Zakryś B., Milanowski R., Empel J., Borsuk P., Kwiatowski J. Two different species of Euglena, E. geniculata and E. myxocylindracea (Euglenophyceae), are virtually enetically and morphological identical // Journal of Phycology. 2002. V. 38. P. 1190–1199. DOI: https://doi.org/10.1046/j.1529-8817.2002.02020.x

Статья поступила в редакцию 20.06.2021
После доработки 11.10.2021
Статья принята к публикации 21.11.2021

Об авторе

Juráň Josef

исследователь (researcher), Южночешский университет, Ческе-Будеёвице, Чешская Республика (University of South Bohemia in České Budějovice, České Budějovice, Czech Republic), Department of Botany, Faculty of Science; Třeboň Experimental Garden and Gene Pool Collections, Institute of Botany of the CAS, Třeboň, Czech Republic

juranj00@prf.jcu.cz

Корреспондентский адрес: Branišovská 1645/31a, 370 05, České Budějovice, Czech Republic; тел. +420-735-700-532.

ССЫЛКА:

Juráň J. Современный взгляд на разнообразие и систематику эвгленовых водорослей: состояние проблемы и актуальные вопросы в области разнообразия, экологии и биогеографии фотосинтезирующих эвгленид // Вопросы современной альгологии. 2021. № 2 (26). P. 114–123. URL: http://algology.ru/1740

DOI – https://doi.org/10.33624/2311-0147-2021-2(26)-114-123

При перепечатке ссылка на сайт обязательна

Уважаемые коллеги! Если Вы хотите получить версию статьи в формате PDF, пожалуйста, напишите в редакцию, и мы ее вам с удовольствием пришлем бесплатно. 
Адрес - info@algology.ru

Modern views on the diversity and taxonomy of Euglenoids.
Current state and challenges for the future in the field of diversity,
ecology, and biogeography of photosynthetic euglenoids

Josef Juráň^1,2

¹University of South Bohemia in České Budějovice (České Budějovice, Czech Republic)
²Třeboň Experimental Garden and Gene Pool Collections, Institute of Botany of the CAS
(Třeboň, Czech Republic)

Photosynthetic euglenoids represent a large group of flagellates, which could be found in most freshwater, marine and brackish habitats, but also in extreme environments with low pH or in moist soil. The existence of this group has been known for a relatively long led to the description of wide morphological variability. In my contribution, I briefly summarize the possible causes of this morphological variability (effect of the environment and phenotypic plasticity during ontogenesis) and current knowledge about the taxonomy of these protist organisms, showing the most recent changes and descriptions of new genera.

Key words: photosynthetic euglenoids; taxonomy; phylogeny; ecology; biogeography

References

1. Bauer D.E., Conforti V., Ruiz L., Gomez N. An in situ test to explore the responses of Scenedesmus acutus and Lepocinclis acus as indicators of the changes in water quality in lowland streams. Ecotoxicology and Environmental Safety. 2012. V. 77. P. 71–78. DOI: https://doi.org/10.1016/j.ecoenv.2011.10.021
2. Bennett M. S., Triemer R.E. A new method for obtaining nuclear gene sequences from field samples and taxonomic revisions of the photosynthetic euglenoids Lepocinclis (Euglena) helicoideus and Lepocinclis (Phacus) horridus (Euglenophyta). Journal of Phycology. 2012. V. 48. P. 254–260. DOI: https://doi.org/10.1111/j.1529-8817.2011.01101.x
3. Bennett M.S., Wiegert K.E., Triemer R.E. Characterization of Euglenaformis gen. nov. and the chloroplast genome of Euglenaformis [Euglena] proxima (Euglenophyta). Phycologia. 2014. V. 53. P. 66–73. DOI: https://doi.org/10.2216/13-198.1
4. Conforti V. Morphological changes of Euglenophyta in response of organic enrichment. Hydrobiologia. 1998. V.369. P. 277–285. DOI: https://doi.org/10.1023/A:1017049910481
5. Conforti V., Ruiz L.B., Leonardi P.I. Ultrastructural Alterations in Lepocinclis acus (Euglenophyta) Induced by Medium with High Organic Matter Content. Frontiers in Ecology and Evolution. 2017. V. 5. P. 141. DOI: https://doi.org/10.3389/fevo.2017.00141
6. Deflandre G. Strombomonas nouveau genere d'euglénacées (Trachelomonas Ehr. pro parte). Archiv für Protistenkunde. 1930 V. 69. P. 551–614.
7. Dujardin, F. Histoire naturelle des Zoophytes, Infusoires, comprenant la physiologie et la clasification de ces animaux et la manière de les étudier à l'aide du microscope. Librarie Encyclopédique de Roret, Paris, 1841. 684 p.
8. Ehrenberg C.G. Neue Beobachtungen über blutartige Erscheinungen in Aegypten, Arabien und Sibirien, nebst einer Uebersicht und Kritik der früher bekannten. Annalen der Physik und Chemie, Ser. 2. 1830. V. 8. P. 477–514.
9. Ehrenberg C.G. Über die Entwickelung und Lebensdauer der Infusionsthiere; nebst ferneren Beiträgen zu einer Vergleichung ihrer organischen Systeme. Abhandlungen der Königlichen Akademie Wissenschaften zu Berlin, Physikalische Klasse. 1832. P. 1–154.
10. Ehrenberg C.G. Dritter Beitrag zur Erkenntniss grosser Organisation in der Richtung des kleinsten Raumes. Abhandlungen der Königlichen Akademie der Wissenschaften zu Berlin. 1834. P.145–336.¨
11. Mereschkowsky K.S. Etjudy nad prostejsimi zivotnymi severa Rossii. Trudy Sankt-Peterburgskago Obshchestva Estestvoisptatele. 1877 V. 8. P. 1–299.
12. Fenchel T., Finlay B.J. The ubiquity of small species: patterns of local and global diversity. BioScience. 2004. V. 54. P. 777–784. DOI: https://doi.org/10.1641/0006-3568(2004)054[0777:TUOSSP]2.0.CO;2
13. Finlay B.J., Corliss J.O., Esteban G., Fenchel T. Biodiversity at the Microbial Level: The Number of Free-Living Ciliates in the Biosphere. The Quarterly Review of Biology. 1996. V.71. P. 221–237. DOI: https://doi.org/10.1086/419370
14. Finlay B.J., Esteban G.F., Fenchel T. Protist Diversity is Different? Protist. 2004. V. 155. P. 15–22. https://doi.org/10.1078/1434461000160
15. Finlay B.J., Fenchel, T. Cosmopolitan metapopulations of free-living microbial eukaryotes. Protist. 2004. V. 155. P. 237–244. DOI: https://doi.org/10.1078/143446104774199619
16. Foissner W. Protist Diversity: Estimates of the Near-Imponderable. Protist. 1999. V. 150. P. 363–368. DOI: https://doi.org/10.1016/S1434-4610(99)70037-4
17. Foissner W. Biogeography and Dispersal of Micro-organisms: A Review Emphasizing Protists. Acta Protozoologica. 2006. V. 45. P. 111–136.
18. Foissner W. Dispersal and Biogeography of Protists: Recent Advances. Japanese Journal of Protozoology. 2007. V. 40. P. 1–16. DOI: https://doi.org/10.18980/jjprotozool.40.1_1
19. Foissner W., Hawksworth D.L. Protist Diversity and Geographical Distribution. Springer, Dordrecht, 2009. 209 p.
20. Fontaneto D. Biogeography of Microscopic Organisms. Is Everything Small Everywhere? Cambridge University Press, New York, 2011. 365 p.
21. Gumińska N., Łukomska‐Kowalczyk M., Chaber K., Zakryś B., Milanowski R. Evaluation of V2 18S rDNA barcode marker and assessment of sample collection and DNA extraction methods for metabarcoding of autotrophic euglenids. Environmental Microbiology. 2021. DOI: https://doi.org/10.1111/1462-2920.15495
22. Guiry M.D., Guiry G.M. AlgaeBase. 2021. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org (date: 15.07.2021).
23. Juráň J., Couté A. African Trachelomonas saccasii found in a European mesotrophic pond (Czech Republic). Implication for euglenoid biogeography and recommendations for euglenoid flagship species. Phytotaxa. 2018. V. 334. P. 201–214. DOI: https://doi.org/10.11646/phytotaxa.334.3.1
24. Karnkowska-Ishikawa A., Milanowski R., Triemer R. E., Zakryś, B. Taxonomic revisions of morphologically similar species from two genera: Euglena (E. granulata and E. velata) and Euglenaria (Eu. anabaena, Eu. caudata, Eu. clavata). Journal of Phycology. 2012. V. 48. P. 729–739. DOI: https://doi.org/10.1111/j.1529-8817.2012.01140.x
25. Karnkowska-Ishikawa A., Milanowski R., Triemer R. E., Zakryś B. A redescription of morphologically similar species from the genus Euglena: E. laciniata, E. sanguinea, E. sociabilis and E. splendens. Journal of Phycology. 2013. V. 49. P. 616–626. DOI: https://doi.org/10.1111/jpy.12072
26. Karnkowska-Ishikawa A., Milanowski R., Zakryś B. The species Euglena deses revisited: New morphological and molecular data. Journal of Phycology. 2011. V. 47. P. 653–661. DOI: https://doi.org/10.1111/j.1529-8817.2011.00982.x
27. Karnkowska‐Ishikawa A., Milanowski R., Kwiatowski J., Zakryś B. Taxonomy of the Phacus oscillans (Euglenaceae) and Its Close Relatives-Balancing Morphological and Molecular Features. Journal of Phycology. 2010. V.46. P. 172–182. DOI: https://doi.org/10.1111/j.1529-8817.2009.00765.x
28. Kim J.I., Linton E.W., Shin W. Morphological and genetic diversity of Euglena deses group (Euglenophyceae) with emphasis on cryptic species. Algae. 2016. V. 31. P. 219–230. DOI: https://doi.org/10.4490/algae.2016.31.9.9
29. Kim J.I., Shin W. Molecular phylogeny and cryptic diversity of the genus Phacus (Phacaceae, Euglenophyceae) and the descriptions of seven new species. Journal of Phycology. 2014. V. 50. P. 948–959. DOI: https://doi.org/10.1111/jpy.12227
30. Kim J.I., Shin W., Triemer R.E. Phylogenetic reappraisal of the genus Monomorphina (Euglenophyceae) based on molecular and morphological data. Journal of Phycology. 2013a. V. 49. P. 82–91. DOI: https://doi.org/10.1111/jpy.12018
31. Kim J.I., Shin W., Triemer, R.E. Cryptic speciation in the genus Cryptoglena (Euglenaceae) revealed by nuclear and plastid SSU and LSU rRNA gene. Journal of Phycology. 2013b. V. 49. P. 92–102. DOI: https://doi.org/10.1111/jpy.12032
32. Kosmala S., Karnkowska A., Milanowski R., Kwiatowski J., Zakryś, B. The phylogenetic and taxonomic position of Lepocinclis fusca comb. nova (=Euglena fusca) (Euglenaceae). Morphological and molecular justification. Journal of Phycology. 2005. V. 41. P. 258–267. DOI: https://doi.org/10.1111/j.1529-8817.2005.00141.x
33. Kosmala S., Karnkowska-Ishikawa A., Milanowski R., Kwiatowski J., Zakryś B. Phylogeny and systematics of species from the genus Euglena (Euglenaceae) with axial, stellate chloroplasts based on morphological and molecular data – New taxa, emended diagnoses and epitypifications. Journal of Phycology. 2009. V. 45. P. 464–481. DOI: https://doi.org/10.1111/j.1529-8817.2009.00653.x
34. Kosmala S., Bereza M., Milanowski R., Kwiatowski J., Zakryś B. Morphological and molecular examination of relationships and epitype establishment of Phacus pleuronectes, Phacus orbicularis and Phacus hamelii. Journal of Phycology. 2007a. V. 43. P.1071–1082. DOI: https://doi.org/10.1111/j.1529-8817.2007.00386.x
35. Kosmala S., Milanowski R., Brzóska K., Pękal, M., Kwiatowski J., Zakryś B. Phylogeny and systematics of the genus Monomorphina (Euglenaceae) based on morphological and molecular data. Journal of Phycology. 2007b. V. 43. P.171–185. DOI: https://doi.org/10.1111/j.1529-8817.2006.00298.x
36. Kristiansen J. Biogeography of freshwater algae. Kluwer, Dordrecht, 1996. 161 p.
37. Linton E.W., Karnkowska-Ishikawa A., Kim J.I., Shin W., Bennett M., Kwiatowski J., Zakryś B., Triemer R.E. Reconstructing euglenoid evolutionary relationships using three genes: Nuclear SSU and LSU, and chloroplast 16S rDNA sequences and the description of Euglenaria gen. nov. (Euglenophyta). Protist. 2010. V. 161. P. 603–619. DOI: https://doi.org/10.1016/j.protis.2010.02.002
38. Łukomska‐Kowalczyk M., Chaber K., Fells A., Milanowski R., Zakryś B. Molecular and morphological delimitation of species in the group of Lepocinclis ovum‐like taxa (Euglenida). Journal of phycology. 2020a. V. 56. P. 283-299. DOI: https://doi.org/10.1111/jpy.12949
39. Łukomska‐Kowalczyk M., Chaber K., Fells A., Milanowski R., Zakryś B. Description of Flexiglena gen. nov. and new members of Discoplastis and Euglenaformis (Euglenida). Journal of Phycology. 2020b. DOI: https://doi.org/10.1111/jpy.13107
40. Łukomska‐Kowalczyk M., Karnkowska A., Krupska M., Milanowski R., Zakryś B. DNA barcoding in autotrophic euglenids: evaluation of COI and 18S rDNA. Journal of Phycology. 2016. V. 52. P. 951–960. DOI: https://doi.org/10.1111/jpy.12439
41. Łukomska-Kowalczyk M., Karnkowska A., Milanowski R., Łach Ł., Zakryś B. Delimiting species in the Phacus longicauda complex (Euglenida) through morphological and molecular analyses. Journal of Phycology. 2015. V. 51. P. 1147–1157. DOI: https://doi.org/10.1111/jpy.12352
42. Marin B., Palm A., Klingberg M., Melkonian M. Phylogeny and taxonomic revision of plastid-containing euglenophytes based on SSU rDNA sequence comparisons and synapomorphic signatures in the SSU rRNA secondary structure. Protist. 2003. V. 154. P. 99–145. DOI: https://doi.org/10.1078/143446103764928521
43. Nannavecchia P., Tolivia A., Conforti V. Ultrastructural alterations in Phacus brachykentron (Euglenophyta) due to excess of organic matter in the culture medium. Ecotoxicology and Environmental Safety. 2014. V. 101. P. 36–41. DOI: https://doi.org/10.1016/j.ecoenv.2013.12.007
44. Nudelman M.A., Leonardi P.I., Conforti V., Farmer M.A., Triemer, R.E. Fine structure and taxonomy of Monomorphina aenigmatica comb. nov (Euglenophyta). Journal of Phycology. 2005. V. 42. P.194–202. DOI: https://doi.org/10.1111/j.1529-8817.2006.00170.x
45. Perty M. Über verticale Verbreitung mikroskopischer Lebensformen. Mittheilungen der Naturforschenden Gesellschaft in Bern. 1849. P. 17–45.
46. Pringsheim E.G. Observation on Some Species of Trachelomonas Grown in Culture. New Phytologist. 1953. V. 52. P. 93–113, 238–266.
47. Shin W., Triemer R. E. Phylogenetic analysis of the genus Euglena (Euglenophyceae) with the particular reference to the type species Euglena viridis. Journal of Phycology. 2004. V. 40. P. 758–771. DOI: https://doi.org/10.1111/j.1529-8817.2004.03142.x
48. Singh K.P. Studies in the genus Trachelomonas. I. Description of six organisms in cultivation. American Journal of Botany. 1956a. V. 43. P. 258–266.
49. Singh K.P. Studies in the genus Trachelomonas. II. Cell structure and reproduction with special reference to T. grandis. American Journal of Botany. 1956b. V. 43. P. 274–280.
50. Triemer R.E., Linton E., Shin W., Nudelman A., Monfils A., Bennett M., Brosnan S. Phylogeny of the euglenales based upon combined SSU and LSU rDNA sequence comparisons and desciption of Discoplastis gen. nov. (Euglenophyta). Journal of Phycology. 2006. V. 42. P. 731–740. DOI: https://doi.org/10.1111/j.1529-8817.2006.00219.x
51. Triemer R.E., Zakryś B. Photosynthetic euglenoids. In: Wehr J.D., Sheath, R.G., Kociolek, J.P. (eds.). Freshwater Algae of North America Amsterdam: Elsevier, 2015. P. 459–483.
52. Stein F. Der Organismus der Infusionsthiere nach eigenen forschungen in systematischere Reihenfolge bearbeitet. III. Abtheilung. Die Naturgeschichte der Flagellaten oder Geisselinfusorien. I. Hälfte, Den noch nicht abgeschlossenen allgemeinen Theil nebst erklärung: Der sämmtlichen Abbildungen enthaltend. Leipzig: Verlag von Wilhelm Engelmann, 1878. 154 p.
53. Wołowski K., Poniewozik M., Juráň J. Morphological variability of loricae in Trachelomonas caudata complex (Euglenophyta). Cryptogamie, Algologie. 2016. V. 37. P. 97–108. DOI: https://doi.org/10.7872/crya/v37.iss2.2016.97
54. Zakryś B., Empel J., Milanowski R., Gromadka R., Borsuk P., Kedzior M., Kwiatowski J. Genetic variability of Euglena agilis (Euglenophyceae). Acta Societaits Botanicorum Poloniae. 2004. V. 73. P. 305–309. DOI: https://doi.org/10.5586/asbp.2004.039
55. Zakryś B., Milanowski R., Empel J., Borsuk P., Kwiatowski J. Two different species of Euglena, E. geniculata and E. myxocylindracea (Euglenophyceae), are virtually enetically and morphological identical. Journal of Phycology. 2002. V. 38. P. 1190–1199. DOI: https://doi.org/10.1046/j.1529-8817.2002.02020.x

Author

Juráň Josef

ORCID – https://orcid.org/0000-0002-9173-9761

University of South Bohemia in České Budějovice, České Budějovice, Czech Republic;
Třeboň Experimental Garden and Gene Pool Collections, Institute of Botany of the CAS, Třeboň, Czech Republic

juranj00@prf.jcu.cz

ARTICLE LINK:

Juráň J. Modern views on the diversity and taxonomy of Euglenoids. Current state and challenges for the future in the field of diversity, ecology, and biogeography of photosynthetic euglenoids. Voprosy sovremennoi algologii (Issues of modern algology). 2021. № 2 (26). P. 114–123. URL: http://algology.ru/1740

DOI – https://doi.org/10.33624/2311-0147-2021-2(26)-114-123

When reprinting a link to the site is required

Dear colleagues! If you want to receive the version of the article in PDF format, write to the editor, please and we send it to you with pleasure for free. 
Address - info@algology.ru

На ГЛАВНУЮ

Карта сайта

КОНТАКТЫ

Email: info@algology.ru

Изготовление интернет сайта
5Dmedia

ЛИЦЕНЗИЯ

Эл N ФС 77-22222 от 01 ноября 2005г.

ISSN 2311-0147