All algae documented so far
are of unknown origin. Here, we provide a taxonomic description of the first
origin-known alga TDX16-DE that arises from the Chroococcidiopsis-like endosymbiotic cyanobacterium
TDX16 by de novo organelle biogenesis after acquiring its green algal host Haematococcus pluvialis’s DNA. TDX16-DE
is spherical or oval, with a diameter of 2.0-3.6 μm, containing typical
chlorophyte pigments of chlorophyll a, chlorophyll b and lutein and reproducing
by autosporulation, whose 18S rRNA gene sequence shows the highest similarity
of 99.7% to that of Chlorella vulgaris.
However, TDX16-DE is only about half the size of C. vulgaris and structurally similar to C. vulgaris only in having a chloroplast-localized pyrenoid, but
differs from C. vulgaris in that 1)
it possesses a double-membraned cytoplasmic envelope but lacks endoplasmic
reticulum and Golgi apparatus; and 2) its nucleus
is enclosed by two sets of envelopes (fourunit membranes). Therefore, based on these characters and the cyanobacterial
origin, we describe TDX16-DE as a new genus and species, Chroococcidiorella tianjinensis gen. et sp. nov., which sets the
basis for multidisciplinary research.
References
[1]
Beijerinck, M.W. (1890) Culturversuche mit Zoochlorellen, Lichen-Engonidien und Anderen Niederen Algen I-III. Botanische Zeitung, 48, 726-740.
[2]
Luo, W., Proschold, T., Bock, C. and Krienitz, L. (2010) Generic Concept in Chlorella-Related Coccoid Green Algae (Chlorophyta, Trebouxiophyceae). Plant Biology, 12, 545-553. https://doi.org/10.1111/j.1438-8677.2009.00221.x
[3]
Fott, B. and Nováková, M. (1969) A Monograph of the Genus Chlorella. The Freshwater Species. In: Fott, B., Ed., Studies in Phycology, Academia, Praha, 10-59.
[4]
Andreyeva, V.M. (1975) Rod Chlorella. Izdat. Nauka, Leningrad, 82 p.
[5]
Maruyama, K. (1977) Classification of Chlorella Strains by Cell Appearance and Group Sera. The Botanical Magazine Tokyo, 90, 57-66.
https://doi.org/10.1007/BF02489469
[6]
Kümmel, H. and Kessler, E. (1980) Physiological and Biochemical Contributions to the Taxonomy of the Genus Chlorella. XIII. Serological Studies. Archives of Microbiology, 126, 15-19. https://doi.org/10.1007/BF00421886
[7]
Takeda, R. (1991) Sugar Composition of the Cell Wall and the Taxonomy of Chlorella (Chlorophyceae). Journal of Phycology, 27, 224-232.
https://doi.org/10.1111/j.0022-3646.1991.00224.x
[8]
Kessler, E. and Huss, V.A.R. (1992) Comparative Physiology and Biochemistry and Taxonomic Assignment of the Chlorella (Chlorophyceae) Strains of the Culture Collection of the University of Texas at Austin. Journal of Phycology, 28, 550-553.
https://doi.org/10.1111/j.0022-3646.1992.00550.x
[9]
Ikeda, T. and Takeda, H. (1995) Species-Specific Differences of Pyrenoids in Chlorella (Chlorophyta). Journal of Phycology, 31, 813-818.
https://doi.org/10.1111/j.0022-3646.1995.00813.x
[10]
Hanagata, N., Karube, I., Chihara, M. and Silva, P.C. (1998) Reconsideration of the Taxonomy of Ellipsoidal Species of Chlorella (Trebouxiophyceae, Chlorophyta), with Establishment of Watanabea gen. nov. Phycological Research, 46, 221-229.
https://doi.org/10.1111/j.1440-1835.1998.tb00117.x
[11]
Friedl, T. (1995) Inferring Taxonomic Positions and Testing Genus Level Assignments in Coccoid Green Algae: A Phylogenetic Analysis of 18S Ribosomal RNA Sequences from Dictyochloropsis reticulata and from Members of the Genus Myrmecia (Chlorophyta, Trebouxiophyceae cl. nov.). Journal of Phycology, 31, 632-639.
https://doi.org/10.1111/j.1529-8817.1995.tb02559.x
[12]
Huss, V., Frank, C., Hartmann, E., Hirmer, M., Kloboucek, A., Seidel, B., Wenzeler, P. and Kessler, E. (1999) Biochemical Taxonomy and Molecular Phylogeny of the Genus Chlorella sensu lato (Chlorophyta). Journal of Phycology, 35, 587-598.
https://doi.org/10.1046/j.1529-8817.1999.3530587.x
[13]
Krienitz, L., Hegewald, E., Hepperle, D., Huss, V., Rohr, T. and Wolf, M. (2004) Phylogenetic Relationship of Chlorella and Parachlorella gen. nov. (Chlorophyta, Trebouxiophyceae). Phycologia, 43, 529-542.
https://doi.org/10.2216/i0031-8884-43-5-529.1
[14]
Karsten, U., Friedl, T., Schumann, R., Hoyer, K. and Lembcke, S. (2005) Mycosporing-Like Amino Acids and Phylogenies in Green Algae: Prasiola and ITS Relatives from the Trebouxiophyceae (Chlorophyta). Journal of Phycology, 41, 557-566.
https://doi.org/10.1111/j.1529-8817.2005.00081.x
[15]
Hoshina, R., Iwataki, M. and Imamura, N. (2010) Chlorella variabilis and Micractinium reisseri sp. nov. (Chlorellaceae, Trebouxiophyceae): Redescription of the Endosymbiotic Green Algae of Paramecium bursaria (Peniculia, Oligohymenophorea) in the 120th Year. Phycological Res., 58, 188-201.
https://doi.org/10.1111/j.1440-1835.2010.00579.x
[16]
Bock, C., Krienitz, L. and Proschold, T. (2011) Taxonomic Reassessment of the Genus Chlorella (Trebouxiophyceae) Using Molecular Signatures (Barcodes), Including Description of Seven New Species. Fottea, 11, 293-312.
https://doi.org/10.5507/fot.2011.028
[17]
Proschold, T., Darienko, T., Silva, P., Reisser, W. and Krienitz, L. (2011) The Systematic of Zoochlorella Revisited Employing an Integrative Approach. Environmental Microbiology, 13, 350-364. https://doi.org/10.1111/j.1462-2920.2010.02333.x
[18]
Neustupa, J., Němcová, Y., Veselá, J., Steinová, J. and Skaloud, P. (2013) Leptochlorella corticola gen. et sp. nov. and Kalinella apyrenoidosa sp. nov.: Two Novel Chlorella-Like Green Microalgae (Trebouxiophyceae, Chlorophyta) from Subaerial Habitats. International Journal of Systematic and Evolutionary Microbiology, 63, 377-387. https://doi.org/10.1099/ijs.0.047944-0
[19]
Skaloud, P., Němcová, Y., Pytela, J., Bogdanov, N.I., Bock, C. and Pickinpaugh, S.H. (2014) Planktochlorella nurekis gen. et sp. nov. (Trebouxiophyceae, Chlorophyta), a novel Coccoid Green Alga Carrying Significant Biotechnological Potential. Fottea, 14, 53-62. https://doi.org/10.5507/fot.2014.004
[20]
Ma, S., Han, B., Huss, V.A.R., Hu, X., Sun, X. and Zhang, J. (2015) Chlorella thermophila (Trebouxiophyceae, Chlorophyta), a Novel Thermo-Tolerant Chlorella Species Isolated from an Occupied Rooftop Incubator. Hydrobiologia, 760, 81-89.
https://doi.org/10.1007/s10750-015-2304-3
[21]
Song, H., Wang, Q., Liu, X., Hu, Y., Long, J., Liu, G. and Hu, Z. (2018) Phylogenic Diversity and Taxonomic Problems of the Dictyosphaerium morphotype within the Parachlorella Clade (Chlorellaceae, Trebouxiophyceae). Journal of Eukaryotic Microbiology, 65, 382-391. https://doi.org/10.1111/jeu.12482
[22]
Song, H., Liu, X., Hu, Y., Wang, Q., Long, J., Liu, G. and Hu, Z. (2018) Coronacoccus hengyangensis gen. et sp. nov., a New Member of Chlorellaceae (Trebouxiophyceae, Chlorophyta) with Radiococcacean Morphology. Phycologia, 57, 363-373.
https://doi.org/10.2216/17-65.1
[23]
Darienko, T., Rad-Menéndez, C., Campbell, C. and Proschold, T. (2019) Are There Any True Marine Chlorella Species? Molecular Phylogenetic Assessment and Ecology of Marine Chlorella-Like Organisms, Including a Description of Droopiella gen. nov. Systematics and Biodiversity, 17, 811-829.
https://doi.org/10.1080/14772000.2019.1690597
[24]
Gonzalez-Esquer, C.R., Smarda, J., Rippka, R., Axen, S.D., Guglielmi, G., Gugger, M. and Kerfeld, C.A. (2016) Cyanobacterial Ultrastructure in Light of Genomic Sequence Data. Photosynthesis Research, 129, 147-157.
https://doi.org/10.1007/s11120-016-0286-2
[25]
Dong, Q.L., Li, Z.W., Xing, X.Y. and Chen, B. (2011) Discovery of an Endophytic Cyanobacterium in Haematococcus pluvialis. Journal of Hebei University of Technology, 40, 1-5. https://doi.org/10.3969/j.issn.1007-2373.2011.03.001
[26]
Dong, Q.L., Xing, X.Y., Wu, H.X., Han, Y., Wei, X.L. and Zhang, S. (2016) Transition of a Prokaryotic Endosymbiotic Cyanobacterium into a Eukaryotic Green alga. Chemical Engineering (China), 44, 1-6.
https://doi.org/10.3969/j.issn.1005-9954.2016.01.001
[27]
Dong, Q.L., Xing, X.Y., Han, Y., Wei, X.L. and Zhang, S. (2020) De Novo Organelle Biogenesis in the Cyanobacterium TDX16 Released from the Green Alga Haematococcus pluvialis. CellBio, 9, 29-84. https://doi.org/10.4236/cellbio.2020.91003
[28]
Dong, Q.L. and Zhao, X.M. (2004) In Situ Carbon Dioxide Fixation in the Process of Natural Astaxanthin Production by a Mixed Culture of Haematococcus pluvialis and Phaffia rhodozyma. Catalysis Today, 98, 537-544.
https://doi.org/10.1016/j.cattod.2004.09.052
[29]
Lichtenthaler, H. (1987) Chlorophylls and Carotenoids: Pigments of Photosynthetic Biomembranes. Methods in Enzymology, 148, 350-382.
https://doi.org/10.1016/0076-6879(87)48036-1
[30]
Zhang, J., Huss, V.A.R., Sun, X., Chang, K. and Pang, D. (2008) Morphology and Phylogenetic Position of a Trebouxiophycean Green Alga (Chlorophyta) Growing on the Rubber Tree, Hevea brasiliensis, with the Description of a New Genus and Species. European Journal of Phycology, 43, 185-193.
https://doi.org/10.1080/09670260701718462
[31]
Govindjee, and Rabinowitch, E. (1960) Two Forms of Chlorophyll a in Vivo with Distinct Photochemical Functions. Science, 132, 355-356.
https://doi.org/10.1126/science.132.3423.355
[32]
Wilhelm, C., Eisenbeis, G., Wild, A. and Zahn, R. (1982) Nanochlorum eucayotum: a Very Reduced Coccoid Species of Marine Chlorophyceae. ZeitschriJt fur Natuiforschung, 37, 107-114. https://doi.org/10.1515/znc-1982-1-219
[33]
Němcová, Y. and Kalina, T. (2000) Cell Wall Development, Microfibril and Pyrenoid Structure in Type Strains of Chlorella vulgaris, C kessleri, C sorokiniana Compared with C luteoviridis (Trebouxiophyceae, Chlorophyta). Algological Studies, 100, 95-105. https://doi.org/10.1127/algol_stud/100/2000/95
[34]
Pribyl, P., Cepák, V. and Zachleder, V. (2013) Production of Lipids and Formation and Mobilization of Lipid Bodies in Chlorella vulgaris. Journal of Applied Phycology, 25, 545-553. https://doi.org/10.1007/s10811-012-9889-y
[35]
Gartner, G., Uzunov, B., Ingolic, E., Kofler, W., Gacheva, G., Pilarski, P., Zagorchev, L., Odjakova, M. and Stoyneva, M. (2015) Мicroscopic Investigations (LM, TEM and SEM) and Identification of Chlorella Isolate R-06/2 from Extreme Habitat in Bulgaria with Strong Biological Activity and Resistance to Environmental Stress Factors. Biotechnology & Biotechnological Equipment, 29, 536-540.
https://doi.org/10.1080/13102818.2015.1013283
[36]
Yamamoto, M., Fujishita, M., Hirata, A. and Kawano, S. (2004) Regeneration and Maturation of Daughter Cell Walls in the Autospore-Forming Green Alga Chlorella vulgaris (Chlorophyta, Trebouxiophyceae). Journal of Plant Research, 117, 257-264.
https://doi.org/10.1007/s10265-004-0154-6
[37]
Bisalputra, T., Ashton, F. and Weier, T. (1966) Role of Dictyosomes in Wall Formation during Cell Division of Chlorella vulgaris. American Journal of Botany, 53, 213-216. https://doi.org/10.1002/j.1537-2197.1966.tb07324.x
[38]
Griffiths, D.A. and Griffiths, D.J. (1969) The Fine Structure of Autotrophic and Heterotrophic Cells of Chlorella vulgaris (Emerson Strain). Plant Cell Physiology, 10, 11-19.
[39]
Gerken, H., Donohoe, B. and Knoshaug, E. (2013) Enzymatic Cell Wall Degradation of Chlorella vulgaris and Other Microalgae for Biofuels Production. Planta, 237, 239-253. https://doi.org/10.1007/s00425-012-1765-0
[40]
Krienitz, L., Huss, V. and Hümmer, C. (1996) Picoplanktonic Choricystis Species (Chlorococcales, Chlorophyta) and Problems Surrounding the Morphologically similar “Nannochloris-Like” Algae. Phycologia, 35, 332-341.
https://doi.org/10.2216/i0031-8884-35-4-332.1
[41]
Krienitz, L., Takeda, H. and Hepperle, D. (1999) Ultrastructure, Cell Wall Composition, and Phylogenetic Position of Pseudodictyosphaerium jurisii (Chlorococcales, Chlorophyta) Including a Comparison with Other Picoplanktonic Green Algae. Phycologia, 38, 100-107. https://doi.org/10.2216/i0031-8884-38-2-100.1
[42]
Hanagata, N., Malinsky-Rushansky, N. and Dubinsky, Z. (1999) Eukaryotic Picoplankton, Mychonastes homosphaera (Chlorophyceae, Chlorophyta), in Lake Kinneret, Israel. Phycological Research, 47, 263-269.
https://doi.org/10.1111/j.1440-1835.1999.tb00307.x
[43]
Lewin, R., Krienitz, L., Goericke, R., Takeda, H. and Hepperle, D. (2000) Picocystis salinarum gen. et sp. nov. (Chlorophyta)—A New Picoplanktonic Green Alga. Phycologia, 39, 560-565. https://doi.org/10.2216/i0031-8884-39-6-560.1
[44]
Henley, W., Hironaka, J., Guillou, L., Buchheim, M., Buchheim, J., Fawley, M. and Fawley, K. (2004) Phylogenetic Analysis of the “Nannochloris-Like” Algae and Diagnoses of Picochlorum oklahomensis gen. et sp. nov. (Trebouxiophyceae, Chlorophyta). Phycologia, 43, 641-652. https://doi.org/10.2216/i0031-8884-43-6-641.1
[45]
Somogyi, B., Felfoldi, T., Solymosi, K., Boddi, B., Marialigeti, K. and Voros, L. (2011) Chloroparva pannonica gen. et sp. nov. (Trebouxiophyceae, Chlorophyta)—A New Picoplanktonic Green Alga from a Turbid, Shallow Soda Pan. Phycologia, 50, 1-10.
https://doi.org/10.2216/10-08.1
[46]
Somogyi, B., Felfoldi, T., Solymosi, K., Flieger, K., Márialigeti, K., Boddi, B. and Voros, L. (2013) One Step Closer to Eliminating the Nomenclatural Problems of Minute Coccoid Green Algae: Pseudochloris wilhelmii, gen. et sp. nov. (Trebouxiophyceae, Chlorophyta). European Journal of Phycology, 48, 427-436.
https://doi.org/10.1080/09670262.2013.854411
[47]
Krienitz, L., Bock, C., Kotut, K. and Proschold, T. (2012) Genotypic Diversity of Dictyosphaerium-morphospecies (Chlorellaceae, Trebouxiophyceae) in African Inland Waters, Including the Description of Four New Genera. Fottea, 12, 231-253.
https://doi.org/10.5507/fot.2012.017
