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http://dx.doi.org/10.4490/algae.2016.31.9.9

Morphological and genetic diversity of Euglena deses group (Euglenophyceae) with emphasis on cryptic species  

Kim, Jong Im (Department of Biology, Chungnam National University)
Linton, Eric W. (Department of Biology, Central Michigan University)
Shin, Woongghi (Department of Biology, Chungnam National University)
Publication Information
ALGAE / v.31, no.3, 2016 , pp. 219-230 More about this Journal
Abstract
The Euglena deses group are common freshwater species composed of E. adhaerens, E. carterae, E. deses, E. mutabilis, and E. satelles. These species are characterized by elongated cylindrical worm-like cell bodies and numerous discoid chloroplasts with a naked pyrenoid. To understand the cryptic diversity, species delimitation and phylogenetic relationships among members of the group, we analyzed morphological data (light and scanning electron microscopy) and molecular data (nuclear small subunit [SSU] and large subunit [LSU] rDNAs and plastid SSU and LSU rDNAs). Bayesian and maximum likelihood analyses based on the combined four-gene dataset resulted in a tree consisting of two major clades within the group. The first clade was composed of two subclades: the E. mutabilis subclade, and the E. satelles, E. carterae, and E. adhaerens subclade. The E. mutabilis subclade was characterized by a lateral canal opening at the anterior end and a single pellicular stria, whereas the E. satelles, E. carterae, and E. adhaerens subclade was characterized by an apical canal opening at the anterior end of the cell and double pellicular striae. The second clade consisted of 20 strains of E. deses, characterizing by a subapical canal opening at the anterior end and double pellicular striae, but they showed cell size variation and high genetic diversity. Species boundaries were tested using a Bayesian multi-locus species delimitation method, resulting in the recognition of five cryptic species within E. deses clade.
Keywords
Euglena deses group; molecular phylogeny; morphology; phylogeny; species delimitation;
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1 Kusel-Fetzmann, E. & Weidinger, M. 2008. Ultrastructure of five Euglena species positioned in the subdivision Serpentes. Protoplasma 233:209-222.   DOI
2 Leedale, G. F. 1967. Euglenoid flagellates. Concepts of modern biology series. Prentice-Hall Inc., Englewood Cliffs, NJ, 242 pp.
3 Leedale, G. F. 1982. Ultrastructure. In Buetow, D. E. (Ed.) The Biology of Euglena, Vol. III. Physiology. Academic Press, New York, pp. 1-27.
4 Lemmermann, E. 1910. Kryptogamenflora der Mark Brandenburg. III. Algen. Verlag von Gebrüder Borntraeger, Leipzig, 712 pp.
5 Lemmermann, E. 1913. Eugleninae. In Pascher, A. (Ed.) Die Süsswasserflora Deutschlands, Österreichs und der Schweiz. H. 2: Flagellatae II. Verlag von Gustav Fisher, Jena, pp. 115-174.
6 Lewis, L. A. & Flechtner, V. R. 2004. Cryptic species of Scenedesmus (Chlorophyta) from desert soil communities of western North America. J. Phycol. 40:1127-1137.   DOI
7 Linton, E. W., Karnkowska-Ishikawa, A., Kim, J. I., Shin, W., Bennett, M. S., Kwiatowski, J., Zakryś, B. & Triemer, R. E. 2010. Reconstructing euglenoid evolutionary relationships using three genes: nuclear SSU and LSU, and chloroplast SSU rDNA sequences and the description of Euglenaria gen. nov. (Euglenophyta). Protist 161:603-619.   DOI
8 Kosmala, S., Milanowski, R., Brzóska, K., Pękala, M., Kwiatowski, J. & Zakryś, B. 2007b. Phylogeny and systematics of the genus Monomorphina (Euglenaceae) based on morphological and molecular data. J. Phycol. 43:171-185.   DOI
9 Shin, W. & Triemer, R. E. 2004. Phylogenetic analysis of the genus Euglena (Euglenophyceae) with particular reference to the type species Euglena viridis. J. Phycol. 40:759-771.   DOI
10 Shin, W. & Boo, S. M. 2001. Ultrastructure of Phacus trypanon (Euglenophyceae) with an emphasis on striated fiber and microtubule arrangement. J. Phycol. 37:95-105.   DOI
11 Popova, T. G. 1966. Euglenophyta 1. Flora Plantarum USSR. 8. Nauka, Moskva-Leningrad, 411 pp. (in Russian).
12 Ehrenberg, C. G. 1838. Die Infusionsthierchen als Vollkommene Organismen. Ein Blick in das Tiefere Organische Leben der Natur. Nebst Einem Atlas von Vierundsechszig Colorirten Kupfertafeln. Gezeichnet vom Verfasser. Verlag von Leopold Voss, Leipzig, 547 pp.
13 Braslavska-Spectorova, E. P. 1937. Pro novii vid biezdjgoutivkovich evglen [Regarding a new species of Euglena without flagella]. J. Inst. Bot. Acad. Sci. R. S. S. Ukraine 11:91-99.
14 Chu, S. P. 1946. Contributions to our knowledge of the genus Euglena. Sinensia 17:75-134.
15 Deflandre, G. & Dusi, H. 1935. Description d’une Euglène nouvelle. Euglena mesnili nov. spec. Arch. Zool. Exp. Gén. 77:12-14.
16 Demchenko, E., Mikhailyuk, T., Coleman, A. W. & Pröschold, T. 2012. Generic and species concepts in Microglena (previously the Chlamydomonas monadina group) revised using an integrative approach. Eur. J. Phycol. 47:264-290.   DOI
17 Ehrenberg, C. G. 1835 (1833). Dritter Beitrag zur Erkenntnis grosser Organisation in der Richtung des kleinsten Raumes. Phys. Abh. K. Akad. Wiss. Berlin 1833:145-336.
18 Fawley, M. W., Fawley, K. P. & Hegewald, E. 2011. Taxonomy of Desmodesmus serratus (Chlorophyceae, Chlorophyta) and related taxa on the basis of morphological and DNA sequence data. Phycologia 50:23-56.   DOI
19 Mainx, F. 1927. Beiträge zur Morphologie und Physiologie der Eugleninen. I. Morphologische Beobachtungen. Methoden und Erfolge der Reinkultur. Arch. Protistenkd. 60:305-414.
20 Lundholm, N., Bates, S. S., Baugh, K. A., Bill, B. D., Connell, L. B., Léger, C. & Trainer, V. L. 2012. Cryptic and pseudocryptic diversity in diatoms: with descriptions of Pseudo-nitzschia hasleana sp. nov. and P. fryxelliana sp. nov. J. Phycol. 48:436-454.   DOI
21 Mann, D. G., McDonald, S. M., Bayer, M. M., Droop, S. J. M., Chepurnov, V. A., Loke, R. E., Ciobanu, A. & du Buf, J. M. H. 2004. The Sellaphora pupula species complex (Bacillariophyceae): morphometric analysis, ultrastructure and mating data provide evidence for five new species. Phycologia 43:459-482.   DOI
22 Marin, B., Palm, A., Klingberg, M. & Melkonian, M. 2003. Phylogeny and taxonomic revision of plastid-containing euglenophytes based on SSU rDNA sequence comparisons and synapomorphic signatures in the SSU rRNA secondary structure. Protist 154:99-145.   DOI
23 Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312-1313.   DOI
24 Škaloud, P., Kynčlová, A., Benada, O., Kofroňová, O. & Škaloudová, M. 2012. Toward a revision of the genus Synura, section Petersenianae (Synurophyceae, Heterokontophyta): morphological characterization of six pseudo-cryptic species. Phycologia 51:303-329.   DOI
25 Škaloud, P., Škaloudová, M., Procházková, A. & Nĕmcová, Y. 2014. Morphological delineation and distribution patterns of four newly described species within the Synura petersenii species complex (Chrysophyceae, Stramenopiles). Eur. J. Phycol. 49:213-229.   DOI
26 Smith, S. W., Overbeek, R., Woese, C. R., Gilbert, W. & Gillevet, P. M. 1994. The genetic data environment: an expandable GUI for multiple sequence analysis. Comput. Appl. Biosci. 10:671-675.
27 Triemer, R. E. 1980. Role of Golgi apparatus in mucilage production and cyst formation in Euglena gracilis (Euglenophyceae). J. Phycol. 16:46-52.   DOI
28 Playfair, G. I. 1921. Australian freshwater flagellates. Proc. Linn. Soc. N. S. W. 46:99-146.
29 Matvienko, O. M. 1938. Materiali do vivtchennia vodorostii URSR (Contributions to the study of the algae of the Ukraine USSR). Tr. N. D. Inst. Bot. Kharkov 3:29-70.
30 Monfils, A. K., Triemer, R. E. & Bellairs, E. F. 2011. Characterization of paramylon morphological diversity in photosynthetic euglenoids (Euglenales, Euglenophyta). Phycologia 50:156-169.   DOI
31 Popova, T. G. 1955. Euglenovyje vodorosli. Opredelitel’ prosnovodnych vodoroslej SSSR, 7 [Euglenophyta. The handbook of freshwater algae of the USSR, 7]. Sovetskaya Nauka, Moskva, 267 pp. (in Russian).
32 Greenwood, S. J., Schnare, M. N., Cook, J. R. & Gray, M. W. 2001. Analysis of intergenic spacer transcripts suggests ‘read-around’ transcription of the extrachromosomal circular rDNA in Euglena gracilis. Nucleic Acids Res. 29:2191-2198.   DOI
33 Triemer, R., Linton, E., Shin, W., Nudelman, A., Monfils, A., Bennett, M. & Brosnan, S. 2006. Phylogeny of the Euglenales based upon combined SSU and LSU rDNA sequence comparisons and description of Discoplastis gen. nov. (Euglenophyta). J. Phycol. 42:731-740.   DOI
34 Walne, P. L., Moestrup, Ø., Norris, R. E., & Ettl, H. 1986. Light and electron microscopical studies of Eutreptiella eupharyngea sp. nov. (Euglenophyceae) from Danish and American waters. Phycologia 25:109-126.   DOI
35 Watanabe, M. M. & Hiroki, M. 1997. NIES-Collection: list of strains. 5th ed. National Institute for Environmental Studies, Tsukuba, 127 pp.
36 Fritsch, F. E., Rich, F. & Stephens, M. E. L. 1930. Contribution to our knowledge of the freshwater algae of Africa. 7. Freshwater algae (exclusive of diatoms) from Griqual-and West. Trans. R. Soc. S. Afr. 18:1-92.   DOI
37 Gojdics, M. 1953. The Genus Euglena. The University of Wisconsin Press, Madison, WI, 268 pp.
38 Jo, B. Y., Shin, W., Kim, H. S., Siver, P. A. & Andersen, R. A. 2013. Phylogeny of the genus Mallomonas (Synurophyceae) and descriptions of five new species on the basis of morphological evidence. Phycologia 52:266-278.   DOI
39 Kim, J. I., Linton, E. W. & Shin, W. 2015. Taxon-rich multigene phylogeny of the photosynthetic euglenoids (Euglenophyceae). Front. Ecol. Evol. 3:98.
40 Karnkowska-Ishikawa, A., Milanowski, R. & Zakryś, B. 2011. The species Euglena deses (Euglenaceae) revisited: new morphological and molecular data. J. Phycol. 47:653-661.   DOI
41 Kim, J. I. & Shin, W. 2007. Ultrastructure of Cryptoglena pigra from Korea. Algae 22:325-331.   DOI
42 Kim, J. I. & Shin, W. 2008. Phylogeny of the Euglenales inferred from plastid LSU rDNA sequences. J. Phycol. 44:994-1000.   DOI
43 Kim, J. I. & Shin, W. 2014. Molecular phylogeny and cryptic diversity of the genus Phacus (Phacaceae, Euglenophyceae) and the descriptions of seven new species. J. Phycol. 50:948-959.   DOI
44 Schmitz, F. 1884. Beiträge zur Kenntnis der Chromatophoren. Pringsh. Jahrb. Wiss. Bot. 15:1-175.
45 Pringsheim, E. G. 1953. Salzwasser-Eugleninen. Arch. Microbiol. 18:149-164.
46 Pringsheim, E. G. 1956. Contributions towards a monograph of the genus Euglena. Nova Acta Leopold. 18:1-168.
47 Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A. & Huelsenbeck, J. P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61:539-542.   DOI
48 Schnare, M. N. & Gray, M. W. 2011. Complete modification maps for the cytosolic small and large subunit rRNAs of Euglena gracilis: functional and evolutionary implications of contrasting patterns between the two rRNA components. J. Mol. Biol. 413:66-83.   DOI
49 Shi, Z. 1989. A new variety of Euglena intermedia inhabiting acid water. Acta Hydrobiol. Sin. 13:287-288.
50 Wermel, E. 1924. Neue order wenig bekannte Protisten XII. Neue order wenig bekannte Flagellaten XI. Beschreibung neuer Flagellaten aus Russland. Arch. Protistenkd. 48:204-206.
51 Wuyts, J., De Rijk, P., Van de Peer, Y., Winkelman, T. & De Wachter, R. 2001. The European large subunit ribosomal RNA database. Nucleic Acid Res. 29:175-177.   DOI
52 Yang, Z. & Rannala, B. 2014. Unguided species delimitation using DNA sequence data from multiple loci. Mol. Biol. Evol. 31:3125-3135.   DOI
53 Zakryś, B. 1986. Contribution to the monograph of Polish members of the genus Euglena Ehrenberg 1830. Nova Hedwig. 42:491-540.
54 Zakryś, B., Cambra-Sanchez, J. & Walne, P. L. 2001. Chloroplast ultrastructure of Euglena cuneata Pringsheim, E. deses Ehrenberg and E. mutabilis (Euglenophyceae): taxonomic significance. Acta Protozool. 40:161-167.
55 Klebs, G. 1883. Über die Organisation einiger Flagellaten-Gruppen und ihre Beziehungen zu Algen und Infusorien. Untersuchungen Bot. Inst. Tübingen 1:233-362.
56 Zakryś, B., Empel, J., Milanowski, R., Gromadka, R., Borsuk, P., Kędzior, M. & Kwiatkowski, J. 2004. Genetic variability of Euglena agilis (Euglenophyceae). Acta Soc. Bot. Pol. 73:305-309.
57 Zakryś, B., Milanowski, R., Empel, J., Borsuk, P., Gromadka, R. & Kwiatowski, J. 2002. Two different species of Euglena, E. geniculata and E. myxocylindracea (Euglenophyceae), are virtually genetically and morphologically identical. J. Phycol. 38:1190-1199.   DOI
58 Kim, J. I., Shin, W. & Triemer, R. E. 2010. Multigene analyses of photosymthetic euglenoids and new family, Phacaceae (Euglenales). J. Phycol. 46:1278-1287.   DOI
59 Kim, J. I., Shin, W. & Triemer R. E. 2013a. Cryptic speciation in the genus Cryptoglena (Euglenaceae) revealed by nuclear and plastid SSU and LSU rRNA gene. J. Phycol. 49:92-102.   DOI
60 Kim, J. I., Shin, W. & Triemer R. E. 2013b. Phylogenetic reappraisal of the genus Monomorphina (Euglenophyceae) based on molecular and morphological data. J. Phycol. 49:82-91.   DOI
61 Kosmala, S., Bereza, M., Milanowski, R., Kwiatowski, J. & Zakryś, B. 2007a. Morphological and molecular examination of relationships and epitype establishment of Phacus pleuronectes, Phacus orbicularis and Phacus hamelii. J. Phycol. 43:1071-1082.   DOI
62 Kosmala, S., Karnkowska-Ishikawa, A., Milanowski, R., Kwiatowski, J. & Zakryś, B. 2009. Phylogeny and systematics of Euglena (Euglenaceae) species with axial, stellate chloroplasts based on morphological and molecular data: new taxa, emended diagnoses and epitypifications. J. Phycol. 45:464-481.   DOI
63 Kosmala, S., Karnkowska, A., Milanowski, R., Kwiatowski, J. & Zakryśc, B. 2005. Phylogenetic and taxonomic position of Lepocinclis fusca comb. nov. (=Euglena fusca) (Euglenaceae): morphological and molecular justification. J. Phycol. 41:1258-1267.   DOI