A taxonomic reassessment of Chlamydomonas meslinii (Volvocales, Chlorophyceae) with a description of Paludistella gen.nov.
Abstract
Chlamydomonas (Volvocales, Chlorophyceae) is a large polyphyletic genus that includes numerous species that should be classified into independent genera. The present study aimed to examine the authentic strain of Chlamydomonas meslinii and related strains based on morphological and molecular data. All the strains possessed an asteroid chloroplast with a central pyrenoid and hemispherical papilla; however, they were different based on cell and stigmata shapes. Molecular phylogenetic analyses based on 18S rDNA, atpB, and psaB indicated that the strains represented a distinct subclade in the clade Chloromonadinia. The secondary structure of ITS-2 supported the separation of the strains into four species. Based on the results, we propose a novel genus, Paludistella, including P. meslinii comb. nov., P. chlorostelatta comb. nov., P. asymmetrica sp. nov., and P. trianguloculus sp. nov.
Keywords
References
Barcytë, D., Hodac, L., Nedbalova, L. & Elster, J. (2018a) Chloromonas arctica sp.nov., a psycrotolerant algae from snow in the high arctic (Chlamydomonadales, Chlorophyta). International Journal of Systematic Evolutionary and Microbiology 68: 851–859.
https://doi.org/10.1099/ijsem.0.002595
Barcytë, D., Hodac, L., Nedbalova, L. & Elster, J. (2018b) Chloromonas svalbardensis n. sp. with insights into the phylogroup Chloromonadinia (Chlorophyceae). The Journal of Eukariotic Microbiology 65: 882–892.
https://doi.org/10.1111/jeu.12633
Bourrelly, P. (1951) Volvocales rares ou nouvelles. Hydrobiologia 3: 251–274.
https://doi.org/10.1007/BF00043717
Buchheim, M.A, Lemieux, C., Otis, C., Gutell, R.R., Chapman, R.L. & Turmel, M. (1996) Phylogeny of Chlamydomonadales (Chlorophyceae): a comparison of ribosomal RNA gene sequences from the nucleus and the chloroplast. Molecular Phylogeneic and Evolution 5: 391–402.
https://doi.org/10.1006/mpev.1996.0034
Buchheim, M.A., Turmel, M., Zimmer, E.A & Chapman, R.L. (1990) Phylogeny of Chlamydomonas (Chlorophyta) based on cladistic analysis of nuclear 18S rRNA sequence data. Journal of Phycology 26: 689–699.
https://doi.org/10.1111/j.0022-3646.1990.00689.x
Chelebieva, E.S., Dantsuk, N.V., Chekanov, K.A., Chubchikova, I.N. Drobetskaya, I.V., Minyuk, G.S., Lobakova, E.S. & Solovchenko, A.E. (2018) Identification and morphological-physiological characterization of astaxanthin producer strains of Haematococcus pluvialis from the Black Sea Region. Applied Biochemistry and Microbiology 54: 639–648.
https://doi.org/10.1134/S0003683818060078
Coleman, A.W. (1994) Molecular delineation of species and syngens in Volvocaceae green algae (Chlorophyta). Journal of Phycology 30: 80–90.
https://doi.org/10.1111/j.0022-3646.1994.00080.x
Coleman, A.W. (2003) ITS2 is a double-edged tool for eukaryote evolutionary comparisons. Trends in Genetics 19: 370–375.
https://doi.org/10.1016/S0168-9525(03)00118-5
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. European Journal of Phycology 47: 264–290.
https://doi.org/10.1080/09670262.2012.678388
Ettl, H. (1976) Die Gattung Chlamydomonas Ehrenberg. Nova Hedwigia Beihefte 49: 1–1122.
Ettl, H. (1983) Chlorophyte I. Phytomonadina. In: Ettl, H., Gerloff, J., Heynig, H. & Mollenhauer, D. (Eds.) Süßwasserflora von Mitteleuropa. Bd. 9. Gustav Fischer, Verlag, Stuttgart, pp. 1–807.
Ettl, H. & Gartner, G. (2014) Syllabus der Boden-, Luftund Flechtenalgen. Springer, Berlin and Heidelberg, 773 pp.
https://doi.org/10.1007/978-3-642-39462-1
Flint, E.A. & Ettl, H. (1966) Some new and uncommon Chlamydomonas species from New Zealand. New Zealand Journal of Botany 4: 418–433.
https://doi.org/10.1080/0028825X.1966.10429059
Fulnečková, J., Hasíková, T., Fajkus, J., Lukešova, A., Eliaš, M., & Sýkorova, E. (2012) Dynamic evolution of telomeric sequences in the green algal order Chlamydomonadales. Genome Biology and Evolution 4: 248–264.
https://doi.org/10.1093/gbe/evs007
Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.
Hamby, R.K., Sims, L., Issel, L. & Zimmer, E (1988) Direct ribosomal RNA sequencing: optimization of extraction and sequencing methods for work with higher plants. Plant Molecular Biology Reporter 6: 175–192.
https://doi.org/10.1007/BF02669591
Hoang, D.T., Olga, C., Arndt, V.H., Bui, Q.M, & Le, S.V. (2018) UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35: 518–522.
hhttps://doi.org/10.1093/molbev/msx281
Hoham, R.W, Berman, J.D, Rogers, H.S., Felio, J.H., Ryba, J.B. & Miller, P.R. (2006) Two new species of green snow algae from Upstate New York, Chloromonas chenangoensis sp. nov. and Chloromonas tughillensis sp. nov. (Volvocales, Chlorophyceae) and the effects of light on their life cycle development. Phycologia 45: 319–330.
https://doi.org/10.2216/04-103.1
Kasai, F., Kawachi, M., Erata, M., Mori, F., Yumoto, K., Sato, M. & Ishimoto, M. (Eds.) (2009) NIES-Collection List of Strains, 8th edition. The Japanese Journal of Phycology (Sorui) 57 (Suppl): 1–350.
Kato, S. (1982) Laboratory culture and morphology of Colacium vesiculosum Ehrb. (Euglenophyceae). The Japanese Journal of Phycology 30: 63–67. [in Japanese with English abstract]
Katoh, K., Misawa, K., Kuma, K. & Miyata, T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acid Research 30: 3059–3066.
https://doi.org/10.1093/nar/gkf436
Kawasaki, Y., Nakada, T. & Tomita, M. (2015) Taxonomic revision of oil-producing green algae, Chlorococcum oleofaciens (Volvocales, Chlorophyceae), and its relatives. Journal of Phycology 51: 1000–1016.
https://doi.org/10.1111/jpy.12343
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35: 1547–1549.
https://doi.org/10.1093/molbev/msy096
Lua, N., Wei, D., Jianga, X., Chena, F. & Yanga, S. (2012) Regulation of lipid metabolism in the snow alga Chlamydomonas nivalis in response to NaCl stress: An integrated analysis by cytomic and lipidomic approaches. Process Biochemistry 47: 1163–1170.
https://doi.org/10.1016/j.procbio.2012.04.011
Masyuk, N.P. & Demchenko, E.N. (2001) A new type of cell division in Chlamydomonadaceae (Chlorophyta). International Journal on Algae 3: 18–30.
https://doi.org/10.1615/InterJAlgae.v3.i2.20
Matsuzaki, R., Nakada, T., Hara, Y. & Nozaki, H. (2010) Light and electron microscopy and molecular phylogenetic analyses of Chloromonas pseudoplatyrhyncha (Volvocales, Chlorophyceae). Phycological Research 58: 202–209.
https://doi.org/10.1111/j.1440-1835.2010.00577.x
Matsuzaki, R., Hara, Y. & Nozaki, H. (2012) A taxonomic revision of Chloromonas reticulata (Volvocales, Chlorophyceae), the type species of the genus Chloromonas, based on multigene phylogeny. Phycologia 51: 74–85.
https://doi.org/10.2216/11-18.1
Matsuzaki, R., Nakada, T., Hara, Y. & Nozaki, H. (2013) Description of Chloromonas kasaiae sp. nov. (Volvocales, Chlorophyceae) based on comparative electron microscopy and molecular data. Phycologia 52: 239–245.
https://doi.org/10.2216/12-083.1
Matsuzaki, R., Hara, Y. & Nozaki, H. (2014) Taxonomic study of snow Chloromonas species (Volvocales, Chlorophyceae) based on light and electron microscopy and molecular analysis of cultured material. Phycologia 53: 293–304.
https://doi.org/10.2216/14-3.1
Matsuzaki, R., Nozaki, H. & Kawachi, M. (2018) Taxonomic revision of Chloromonas nivalis (Volvocales, Chlorophyceae) strains, with the new description of snow-inhabiting Chloromonas species. PLOS One 13: e0193603.
https://doi.org/10.1371/journal.pone.0193603
Muramoto, K., Nakada, T., Shitara, T., Hara, Y., & Nozaki, H. (2010) Re-examination of the snow algal species Chloromonas miwae (Fukushima) Muramoto et al., comb. nov. (Volvocales, Chlorophyceae) from Japan, based on molecular phylogeny and cultured material. European Journal of Phycology 45: 27–37.
https://doi.org/10.1080/09670260903272607
Nakada, T., Suda, S. & Nozaki, H. (2007) a taxonomic study of Hafniomonas (Chlorophyceae) based on a comparative examination of cultured material. Journal of Phycology 43: 397–411.
https://doi.org/10.1111/j.1529-8817.2007.00328.x
Nakada, T., Misawa, K. & Nozaki, H. (2008) Molecular systematics of Volvocales (Chlorophyceae, Chlorophyta) based on exhaustive 18S rRNA phylogenetic analyses. Molecular Phylogenetics and Evolution 48: 281–291.
https://doi.org/10.1016/j.ympev.2008.03.016
Nakada, T., Shinkawa, H., Ito, T. & Tomita, M. (2010) Recharacterization of Chlamydomonas reinhardtii and its relatives with new isolates from Japan. Journal of Plant Research 121: 67–78.
https://doi.org/10.1007/s10265-009-0266-0
Nakada, T., Matsuzaki, R., Krienitz, L., Tomita, M. & Nozaki, H. (2015) Taxonomic reassessment of strains formerly classified as Chloromonas insignis (Volvocales, Chlorophyceae) and description of Gleomonas anomalipyrenoides sp.nov. Acta Phytotaxonomica et Geobotanica 66: 23–33.
https://doi.org/10.18942/apg.KJ00009868503
Nakada, T., Tomita, M., Wu, J.T. & Nozaki, H. (2016) Taxonomic revision of Chlamydomonas subg. Amphichloris (Volvocales, Chlorophyceae), with resurrection of the genus Dangeardinia and description of Ixipapillifera gen. nov. and Rhysamphichloris gen. nov. Journal of Phycology 52: 283–304.
https://doi.org/10.1111/jpy.12397
Nakada, T., Tsuchida, Y., & Tomita, M. (2019) Improved taxon sampling and multigene phylogeny of unicellular Chlamydomonads closely related to the colonial Volvocalean lineage Tetrabaenaceae-Goniaceae-Volvocaceae (Volvocales, Chlorophyceae). Molecular Phylogenetic and Evolution 130: 1–8.
https://doi.org/10.1016/j.ympev.2018.09.013
Nakayama, T., Marin, B., Kranz, H.D., Surek, B., Huss, V.A., Inouye, I. & Melkonian, M. (1998) The basal position of scaly green flagellates among the green algae (Chlorophyta) SSU rRNA sequences. Protist 149: 367–380.
https://doi.org/10.1016/S1434-4610(98)70043-4
Nakazawa, A. & Nozaki, H. (2004) Phylogenetic analysis of the Tetrasporalean genus Asterococcus (Chlorophyceae) based on 18S ribosomal RNA gene sequences. Journal of Japanese Botany 79: 255–261.
Nguyen, L., Heiko, A.S., Arndt, V.H., & Bui, Q.M. (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution 32: 268–274.
https://doi.org/10.1093/molbev/msu300
Novis, P.M., Hoham, R.W. Beer, T. & Dawson, M. (2008) Two snow species of quadriflagellate green alga Chlainomonas (Chlorophyta, Volvocales): Ultrastucture and phylogenetic position within the Chloromonas clade. Journal of Phycology 44: 1001–1012.
https://doi.org/10.1111/j.1529-8817.2008.00545.x
Nozaki, H., Ohta, N., Takano, H., & Watanabe, M.M. (1999) Re-examination of phylogenetic relationships within the colonial Volvocales (Chlorophyta): an analysis of atpB and rbcL gene sequences. Journal of Phycology 35: 104–112.
https://doi.org/10.1046/j.1529-8817.1999.3510104.x
Nozaki, H., Misawa, K., Kajita, T., Kato, M., Nohara, S. & Watanabe, M.M. (2000) Origin and evolution of colonial Volvocales (Chlorophyceae) as inferred from multiple, chloroplast gene sequences. Molecular Phylogenetics and Evolution 17: 256–268.
https://doi.org/10.1006/mpev.2000.0831
Nozaki, H., Takahara, M., Nakazawa, A., Kita, Y., Yamada, T., Takano, H., Kawano, S. & Kato, M. (2002) Evolution of rbcl group IA introns and intron open reading frames within the colonial Volvocales (Chlorophyceae). Molecular Phylogenetics and Evolution 23: 326–338
https://doi.org/10.1016/S1055-7903(02)00030-1
Nozaki, H., Nakada, T. & Watanabe, S. (2010) Evolutionary origin of Gloeomonas (Volvocales, Chlorophyceae), based on ultrastructure of chloroplasts and molecular phylogeny. Journal of Phycology 46: 195–201.
https://doi.org/10.1111/j.1529-8817.2009.00773.x
Nylander, J.A.A. (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.
Pröschold, T., Marin, B., Osser, U.G. & Melkonian, M. (2001) Molecular phylogeny and taxonomic revision of Chloromonas (Chlorophyta). I. Emendation of Chlamydomonas Ehrenberg and Chloromonas Gobi, and description of Oogamochlamys gen. nov. and Lobochlamys gen. nov. Protist 152: 265–300.
https://doi.org/10.1078/1434-4610-00068
Pröschold, T., Harris, E.H. & Coleman, A.W. (2005) Portrait of a species Chlamydomonas reinhardtii. Genetics 170: 1601–1610.
https://doi.org/10.1534/genetics.105.044503
Pröschold, T. & Silva, P.C (2007) Proposal to changes the listed type of Chlamydomonas Ehrenb., nom. cons. (Chlorophyta). Taxon 56: 595–596.
https://doi.org/10.1002/tax.562033
Pröschold, T. & Leliaert, F. (2007) Systematics of the green algae: Conflict of classic and modern approaches. In: Brodie, J. & Lewis, J. (Eds.) Unravelling the algae: The past, present, and future of the algae systematics. CRC Press, Taylor and Francis, Boca Raton, London, New York, pp. 123–153.
https://doi.org/10.1201/9780849379901.ch7
Pröschold, T., Darienko, T., Krienitz, L. & Coleman, A.W. (2018) Chlamydomonas schloesseri sp. nov. (Chlamydophyceae, Chlorophyta) revealed by morphology, autolysin cross experiments, and multiple gene analyses. Phytotaxa 362: 21–38.
https://doi.org/10.11646/phytotaxa.362.1.2
Rambaut, A. (2012) FigTree v1.4.0: Tree Figure Drawing Tool. Available from: http://tree.bio.ed.ac.uk/software/figtree/ (accessed 5 December 2018)
Remias, D., Wastian, H., Lutz, C. & Leya, T. (2013) Insights into the biology and phylogeny of Chloromonas polyptera (Chlorophyta), an alga causing orange snow in Maritime Antartica. Antartic Science 25: 648–656.
https://doi.org/10.1017/S0954102013000060
Reuter, J.S. & Mathews, D.H. (2010) RNAstructure: software for RNA secondary structure prediction and analysis. BMC Bioinformatics 11: 129.
https://doi.org/10.1186/1471-2105-11-129
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Hohna, 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. Systematic Biology 61: 539–542.
https://doi.org/10.1093/sysbio/sys029
Spurr, A.R. (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. Journal of Ultrastructure Research 26: 31–43.
https://doi.org/10.1016/S0022-5320(69)90033-1
Swofford, D.L. (2002) PAUP* Version 4.0 b10. Phylogenetic Analysis Using Parsimony (* and Other Methods). Sinauer, Sunderland, MA.
Takahashi, S., Tomita, M. & Nakada, T. (2018) Morphology and phylogeny of a Japanese strain of Chlamydomonas augustae (Volvocales, Chlorophyceae). The Journal of Japanese Botany 93: 317–321.
Wiersema, J.H., McNeill, J., Turland, N.J., Barrie, F.R., Buck, W.R., De moulin, V., Greuter, W., Hawksworth, D., Herendeen, P., Knapp, S., Marhold, K., Prado, J., van Reine, W.P. & Smith, G.F. (2015) International code of nomenclature for algae, fungi, and plants (Melbourne Code) adopted by the eighteenth International Botanical Congress Melbourne, Australia, July 2011. Appendices II–VIII. Regnum Veg. 157. pp. 1–492.
Wolf, M., Chen, S., Song, J., Ankenbrand, M. & Müller, T. (2013) Compensatory base changes in ITS2 secondary structures correlate with the biological species concept despite intragenomic variability in ITS2 sequences – a proof of concept. PLoS-One 8: e66726
https://doi.org/10.1371/journal.pone.0066726
Yoshida, M., Nakayama, T. & Inouye, I. (2009) Nuclearia thermophila sp. nov. (Nucleariidae), a new nucleariid species isolated from Yunoko Lake in Nikko (Japan). European Journal of Protistology 45: 147–155.
https://doi.org/10.1016/j.ejop.2008.09.004
Yumoto, K., Kasai, F. & Kawachi, M. (2013) Taxonomic re-examination of Chlamydomonas strains maintained in the NIES collection. Microbiology Culture Collection 29: 1–12.
Zuker, D.J. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research 31: 3406–3415
https://doi.org/10.1093/nar/gkg595
DOI: https://doi.org/10.11646/phytotaxa.432.1.6
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