Skip to main content
Log in

Species Delimitation and Cryptic Diversity Analysis of Parachlorella-Сlade Microalgae (Chlorophyta)

  • EXPERIMENTAL ARTICLES
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

This article discusses the system of green microalgae of the clade Parachlorella, based on morphological, ecological, and molecular genetic data. The diagnostic characteristics of the selected genera and species and the systematic position of some taxa are discussed. Phylogenetic analysis of the Parachlorella-clade has shown that, despite the relative simplicity of morphology, it is characterized by high cryptic diversity. The polyphyletic nature of the genus Dictyosphaerium and some species (D. libertatis, D. ehrenbergianum, Compactochlorella kochii, Mucidosphaerium pulchellum, M. palustre, and Closteriopsis acicularis) was shown. Theuse of the intron as a universal criterion for closely related species was effective for representatives of groups II, IV, VII, and VIII, as well as for strains of the species Compactochlorella kochii and D. libertatis. The application of the classical CBC approach, based on the search for CBC in conservative ITS2 regions, was successful only for the representatives of group II. The results of analysis of genetic distances and the GMYC, PTP, and ABGD species delimitation algorithms are not universal tools for determining species boundaries and need to be confirmed by other characteristics (cell shape, ability to form colonies, the way the cells attach to hyaline interconnecting strands, the type of chloroplast, the number of pyrenoids, the presence of mucilage, the presence/absence of introns, the level of genetic differences, the presence of CBC in ITS1 and ITS2, the habitat). Due to the combined use of morphological, ecological and genetic features, it was possible to characterize 11 groups and 2 phylogenetic lines within the clade Parachlorella and to make assumptions about the division of genera and species within the selected groups.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 4.

Similar content being viewed by others

REFERENCES

  1. Aslam, Z., Shin, W., Kim, M.K., Im, W.-T., and Lee, S.-T., Marinichlorella kaistiae gen. et sp. nov. (Trebouxiophyceae, Chlorophyta) based on polyphasic taxonomy, J. Phycol., 2007, vol. 43, pp. 576–584.

    Article  Google Scholar 

  2. Belcher, J.H. and Swale, E.M.F., Some Chlorococcales new to Britain, Brit. Phycol. Bull., 1962, vol. 2, pp. 121–125.

    Article  Google Scholar 

  3. Bock, C., Pröschold, T., and Krienitz, L., Two new Dictyosphaerium-morphotype lineages of the Chlorellaceae (Trebouxiophyceae): Heynigia gen. nov. and Hindakia gen. nov., Eur. J. Phycol., 2010, vol. 45, pp. 267–277.

    Article  CAS  Google Scholar 

  4. Bock, C., Pažoutová, M., and Krienitz, L., Phylogenetic position of Coronastrum ellipsoideum and description of Parachlorella hussii sp. nov., Biologia, 2011a, vol. 66/4, pp. 585–594.

    Article  Google Scholar 

  5. Bock, C., Pröschold, T., and Krienitz, L., Updating the genus Dictyosphaerium and description of Mucidosphaerium gen. nov. (Trebouxiophyceae) based on morphological and molecular data, J. Phycol., 2011b, vol. 47, pp. 638–652.

    Article  CAS  Google Scholar 

  6. Caisová, L., Marin, B., and Melkonian, M., A consensus secondary structure of ITS2 in the Chlorophyta identified by phylogenetic reconstruction, Protist, 2013, vol. 164, pp. 482–496.

    Article  Google Scholar 

  7. Coleman A.W. Is there a molecular key to the level of “biological species” in eukaryotes? A DNA guide, Mol. Phylogenet. Evol., 2009, vol. 50, pp. 197–203.

    Article  CAS  Google Scholar 

  8. Coleman, A.W., The significance of a coincidence between evolutionary landmarks found in mating affinity and a DNA sequence, Protist, 2000, vol. 151, pp. 1–9.

    Article  CAS  Google Scholar 

  9. Coleman, A.W., ITS2 is a double-edged tool for eukaryote evolutionary comparisons, Trends Genet., 2003, vol. 19, pp. 370–375.

    Article  CAS  Google Scholar 

  10. Coleman, A.W., Nuclear rRNA transcript processing versus internal transcribed spacer secondary structure, Trends Genet., 2015, vol. 31, pp. 157–163.

    Article  CAS  Google Scholar 

  11. Drummond, A.J., Nicholls, G.K., Rodrigo, A.G., and Solomon, W., Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data, Genetics, 2002, vol. 161, pp. 1307–1320.

    Article  CAS  Google Scholar 

  12. Fawley, M.W., Dean, M.L., Dimmer, S.K., and Fawley, K.P., Evaluating the morphospecies concept in the Selenastraceae (Chlorophyceae, Chlorophyta), J. Phycol., 2006, vol. 42, pp. 142–154.

    Article  Google Scholar 

  13. Fujisawa, T. and Barraclough, T.G., Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets, Syst. Biol., 2013, vol. 62, pp. 707–724.

    Article  Google Scholar 

  14. Gaisina, L.A., Fazlutdinova, A.I., and Kabirov, R.R., Sovermennye metody vydeleniya i kul’tivirovaniya vodoroslei (Modern Methods for Isolation and Cultivation of Algae), Ufa: BGPU, 2008.

  15. Gaonkar, C.C., Piredda, R., Minucci, C., Mann, D., Montresor, M., Sarno, D., and Kooistra, W.H.C.F., Annotated 18S and 28S rDNA reference sequences of taxa in the planktonic diatom family Chaetocerotaceae, PLoS One, 2018, vol. 13, e0208929. https://doi.org/10.1371/journal.pone.0208929

    Article  PubMed  PubMed Central  Google Scholar 

  16. Guiry, M.D. and Guiry, G.M., AlgaeBase, World-wide electronic publication, National Univ. Ireland, Galway, 2021. http://www.algaebase.org.

    Google Scholar 

  17. Jao, C.-C., Wei, Y.X., and Hu, H.J., Dicloster, a new genus of Chlorococcales, Acta Hydrobiol. Sin., 1975, vol. 6, pp. 115–116.

    Google Scholar 

  18. Hoshina, R., Iwataki, M., and Imamura, N., Chlorella variabilis and Micractinium reisseri sp. nov. (Chlorellaceae, Trebouxiophyceae): redescription of the endosymbiotic green algae of Paramecium bursaria (Peniculia, Oligohymenophorea) in the 120th year, Phycol. Res., 2010, vol. 58, pp. 188–210.

    Article  CAS  Google Scholar 

  19. Krienitz, L., Hegewald, E.H., Hepperle, D., Huss, V.A.R., Rohr, T., and Wolf, M., Phylogenetic relationship of Chlorella and Parachlorella gen. nov. (Chlorophyta, Trebouxiophyceae), Phycologia, 2004, vol. 43, pp. 529–542.

    Article  Google Scholar 

  20. Krienitz, L., Bock, C., Kotut, K., and Pröschold, T., Genotypic diversity of Dictyosphaerium-morphospecies (Chlorellaceae, Trebouxiophyceae) in African inland waters, including the description of four new genera, Fottea, 2012, vol. 12, pp. 231–253.

    Article  Google Scholar 

  21. Krienitz, L., Bock, C., Luo, W., and Pröschold, T., Polyphyletic origin of the Dictyosphaerium-morphotype within Chlorellaceae (Trebouxiophyceae), J. Phycol., 2010, vol. 46, pp. 559–563.

    Article  CAS  Google Scholar 

  22. Krivina, E.S. and Temraleeva, A.D., Identification problems and cryptic diversity of Chlorella-clade microalgae (Chlorophyta), Microbiology (Moscow), 2020, vol. 89, pp. 720–732.

    Article  CAS  Google Scholar 

  23. Luo, W., Pröschold, T., Bock, C., and Krienitz, L., Generic concept in Chlorella-related coccoid green algae (Chlorophyta, Trebouxiophyceae), Plant Biol., 2010, vol. 12, pp. 545–553.

    Article  CAS  Google Scholar 

  24. Puillandre, N., Lambert, A., Brouillet, S., and Achaz, G., ABGD, Automatic Barcode Gap Discovery for primary species delimitation, Mol. Ecol., 2012, vol. 21, pp. 1864–1877.

    Article  CAS  Google Scholar 

  25. Škaloud, P., Němcová, Y., Pytela, J., Bogdanov, N.I., Bock, C., and Pickinpaugh, S.H., Planktochlorella nurekis gen. et sp. nov. (Trebouxiophyceae, Chlorophyta), a novel coccoid green alga carrying significant biotechnological potential, Fottea, 2014, vol. 14, pp. 53–62.

    Article  Google Scholar 

  26. Song, H., Liu, X., Hu, Y., Wang, Q., Long, J., Liu, G., and Hu, Z., Coronacoccus hengyangensis gen. et sp. nov., a new member of Chlorellaceae (Trebouxiophyceae, Chlorophyta) with Radiococcacean morphology, Phycologia, 2018a, vol. 57, pp. 363–373.

    Article  CAS  Google Scholar 

  27. Song, H., Qinghua Wang, Q., Liu, X., Hu, Y., Long, J., Guoxiang Liu, G., and Hu, Z., Phylogenic diversity and taxonomic problems of the Dictyosphaerium morphotype within the Parachlorella clade (Chlorellaceae, Trebouxiophyceae), J. Eukaryot. Microbiol., 2018b, vol. 65, pp. 382–391.

    Article  Google Scholar 

  28. Temraleeva, A., Moskalenko, S., Mincheva, E., Bukin, Y., and Sinetova, M., Spongiosarcinopsis terrestris gen. et sp. nov. (Chlorophyta, Chlorophyceae): a new genus of green algae from gray forest soil, Russia, Phytotaxa, 2018, vol. 376, pp. 291–300.

    Article  Google Scholar 

  29. Ustinova, I., Krienitz, L., and Huss, V.A.R., Closteriopsis acicularis (G.M. Smith) Belcher et Swale is a fusiform alga closely related to Chlorella kessleri Fott et Nováková (Chlorophyta, Trebouxiophyceae), Eur. J. Phycol., 2001, vol. 36, pp. 341–351.

    Article  Google Scholar 

  30. Yamamoto, M., Kurihara, I., and Kawano, S., Late type daughter cell wall synthesis in one of the Chlorellaceae, Parachlorella kessleri (Chlorophyta, Trebouxiophyceae), Planta, 2005, vol. 221, pp. 766–775.

    Article  CAS  Google Scholar 

  31. Zhu, X.C., Chen, J., Chen, R., Jiang, L.Y., and Qiao, G.X., DNA barcoding and species delimitation of Chaitophorinae (Hemiptera, Aphididae), ZooKeys, 2017, vol. 656, pp. 25–50.

    Article  Google Scholar 

  32. Zou, S., Fei, C., Song, J., Bao, Y., He, M., and Wang, C., Combining and comparing coalescent, distance and character-based approaches for barcoding microalgaes: a test with Chlorella-like species (Chlorophyta), PLoS One, 2016a, vol. 11. e0153833.

    Article  Google Scholar 

  33. Zou, S., Fei, C., Wang, C., Gao, Z., Bao, Y., He, M., and Wang, C., How DNA barcoding can be more effective in microalgae identification: a case of cryptic diversity revelation in Scenedesmus (Chlorophyceae), Sci. Rep., 2016b, vol. 6, pp. 1–13.

    Article  CAS  Google Scholar 

Download references

ACKNOWLEDGMENTS

The authors are grateful to M.A. Sinetova, the Chief of the IPPAS Collection of Microalgae and Cyanobacteria, the Institute of Plant Physiology, Russian Academy of Sciences, for providing the strains.

Funding

The cultivation and microscopy of ACSSI strains and literature analysis were supported by the Russian Foundation for Basic Research, project no. 19-34-60002; molecular phylogenetic studies were supported by the Russian Science Foundation, project no. 19-74-00030.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. S. Krivina.

Ethics declarations

The authors declare that they have no conflict of interest.

The authors declare that they have no conflict of interest. The article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by E. Makeeva

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Krivina, E.S., Temraleeva, A.D. & Bukin, Y.S. Species Delimitation and Cryptic Diversity Analysis of Parachlorella-Сlade Microalgae (Chlorophyta). Microbiology 90, 455–469 (2021). https://doi.org/10.1134/S0026261721040081

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261721040081

Keywords:

Navigation