Open Access Open Access  Restricted Access Subscription or Fee Access


DOI: http://dx.doi.org/10.11646/phytotaxa.192.1.1

Polyphasic characterization of four species of Pseudanabaena (Oscillatoriales, Cyanobacteria) from China and insights into polyphyletic divergence within the Pseudanabaena genus

Gongliang Yu, Mengling Zhu, Youxin Chen, Qianqian Pan, Wenbo Chai, Renhui Li

Abstract


Current cyanobacterial taxonomic studies are mainly performed through polyphasic characterization at the genus and/or species levels. In this study, eleven Pseudanabaena strains isolated in China were taxonomically and phylogenetically evaluated by investigating several characteristics, including morphological features, cellular ultrastructures, pigment composition, and 16S rRNA gene sequences. The strains were identified as four morphospecies, namely, Pseudanabaena mucicola, P. galeata, P. limnetica, and P. minima. The cellular ultrastructures of these species showed that peripheral thylakoids with 4‒8 parallel layers were parietally distributed. Phylogenetic results based on 16S rRNA gene sequences indicated that most of the Pseudanabaena strains used in this study, including the eleven from China and three Pseudanabaena catenata strains from GenBank, gathered into one large cluster that represents the core of the genus Pseudanabaena. Several Pseudanabaena species/strains that represent different extreme environments were phylogenetically located outside the main stream cluster and should be removed under the genus Pseudanabaena on the basis of the role of the main stream species. Limnothrix strains were divided into two clades, and the taxonomic solution for these clades was discussed. This study is the first to report on the morphology and phylogeny of Pseudanabaena species in China, providing new insights into the taxonomy of the genera Pseudanabaena and Limnothrix.


Keywords


China, cyanobacteria, Limnothrix, morphology, phylogeny, Pseudanabaena, taxonomy

Full Text:

PDF/A (4.30 MB)

References


Acinas, S.G., Haverkamp, T.H.A., Huisman, J. & Stal, L.J. (2009) Phenotypic and genetic diversification of Pseudanabaena spp. (cyanobacteria). ISME Journal 3: 31–46.

http://dx.doi.org/10.1038/ismej.2008.78

An, G.S. (1992) Validation of new species names of blue-green algae Cyanophyta from Korea. Fragmenta Floristica et Geobotanica 37(2): 407–416.

Anagnostidis, K. (2001) Nomenclatural changes in cyanoprokaryotic order Oscillatoriales. Preslia, Praha 73: 359–375.

Anagnostidis, K. & Komárek, J. (1988) Modern approach to the classification system of cyanophytes 3. Oscillatoriales. Algological Studies 50–53: 327–472.

Böcher, T.W. (1949) Studies on the sapropelic flora of the lake Flyndersø with special reference to the Oscillatoriaceae. Kongelige Danske Videnskabernes Selskab Biologiske Meddelelser 21: 1–46.

Casamatta, D.A., Johansen, J.R., Vis, M.L. & Broadwater, S.T. (2005) Molecular and morphological characterization of ten polar and near-polar strains within the Oscillatoriales (Cyanobacteria). Journal of Phycology 41: 421–438.

http://dx.doi.org/10.1111/j.1529-8817.2005.04062.x

Chang, T. (1988) Morphological remarks on Pseudanabaena mucicola (Huber-Pestalozzi et Naumann) (Bourrelly) Chang. Algological Studies 80: 1–4.

Desikachary, T.V. 1959. Cyanophyta. Indian Council of Agriculture Research, New Delhi, pp. 81–132.

DeVries, S.L., Liu, W., Wan, N., Zhang, P. & Li, X. (2012) Biodegradation of MIB, geosmin and microcystin-LR in sand columns containing Taihu lake sediment. Water Science and Technology: Water Supply 12(5): 691–698.

http://dx.doi.org/10.2166/ws.2012.043

Dignum, M., Hoogveld, H.L., Matthijs, H.C.P., Laanbroek, H.J. & Pel, R. (2004) Detecting the phosphate status of phytoplankton by enzyme-labelled fluorescence and flow cytometry. FEMS Microbiology Ecology 48: 29–38.

http://dx.doi.org/10.1016/j.femsec.2003.12.007

Fritsch, F.E. (1945) The Structure and Reproduction of the Algae. Cambridge University Press, Cambridge, 939 pp.

Geitler, L. (1932) Cyanophyceae. In: Rabenhorst, L. (Ed.) Kryptogamen Flora von Deutschland, Osterreich und der Schweiz 14. Akademische Verlagsgesellschaft, Leipzig, pp. 130–159.

Gomont, M. (1892) Monographie des Oscillariées (Nostocacées homocystées). [Séries 7] Annales des Sciences Naturelles, Botanique 15: 263–368.

Goor, A.C.J. van (1918) Zur Kenntnis der Oscillatoriaceen. Reçueil des Travaux Botaniques Néerlandais 15: 255–262.

Guindon, S. & Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systems Biology 52: 696–704.

http://dx.doi.org/10.1080/10635150390235520

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.

Huber-Pestalozzi, G. & Naumann, E. (1929) Phormidium mucicola Naumann et Huber, ein Epibiont in der Gallerte pflanzlicher und tierischer Planktonorganismen. Berichte der Deutschen Botanischen Gesellschaft 47(1): 67–76.

http://dx.doi.org/10.1111/j.1438-8677.1929.tb01573.x

Kasai, F., Kawachi, M., Erata, M., Mori, F., Yumoto, K., Sato, M. & Ishimoto, M. (2009) NIES-Collection, List of Strains, 8th edn. The Japanese Journal of Phycology 57(1): 216–217.

Kehoe, D.M. & Gutu, A. (2006) Responding to color: the regulation of complementary chromatic adaptation. Annual Review of Plant Biology 57: 127–150.

http://dx.doi.org/10.1146/annurev.arplant.57.032905.105215

Kim, S.G., Rhee, S.K., Ahn, C.Y., Ko, S.R., Choi, G.G., Bae, J.W., Park, Y.H. & Oh, H.M. (2006) Determination of cyanobacterial diversity during algal blooms in Daechung Reservoir, Korea, on the basis of cpcBA intergenic spacer region analysis. Applied and Environmental Microbiology 72(5): 3252–3258.

http://dx.doi.org/10.1128/AEM.72.5.3252-3258.2006

Kling, H.J. & Watson, S. (2003) A new planktic species of Pseudanabaena (Cyanoprokaryota, Oscillatoriales) from North American large lakes. Hydrobiologia 502: 383–388.

http://dx.doi.org/ 10.1023/B:HYDR.0000004295.11437.df

Kling, H.J., Laughinghouse IV, H.D., Šmarda, J., KomáreK, J., Acreman, J., Bruun, K., Watson, S.B. & Chen, F. (2012) A new red colonial Pseudanabaena (Cyanoprokaryota, Oscillatoriales) from North American large lakes. Fottea Olomouc 12(2): 327–339.

Komárek, J. (1974) Taxonomische Bemerkungen zu einigen Arten der Mikroflora der Teiche in Böhmen. Acta Scientiarum Naturalium Musei Bohemici Meridionalis Ceské Budejovice 14: 161–190.

Komárek, J. (2003) Planktic oscillatorialean cyanoprokaryotes (short review according to combined phenotype and molecular aspects). Hydrobiologia 502: 367–382.

http://dx.doi.org/10.1023/B:HYDR.0000004294.17755.fe

Komárek, J. & Anagnostidis, K. (2005) Cyanoprokaryota 2. Teil: Oscillatoriales. Elsevier GmbH, Heifelberg, 70 pp.

Kützing, F.T. (1833) Beitrag zur Kenntniss über die Entstehung und Metamorphose der niedern vegetabilischen Organismen, nebst einer systematischen Zusammenstellung der hieher gehörigen niedern Algenformen. Linnaea 8: 335–384.

Kützing, F.T. (1846) Tabulae phycologicae; oder, Abbildungen der Tange. Vol. I. Gedruckt auf kosten des verfassers (in commission bei W. Köhne), Nordhausen, 54 pp.

http://dx.doi.org/10.5962/bhl.title.4971

Lauterborn, R. (1915) Die sapropelische Lebewelt. Ein Beitrag zur Biologie des Faulschlammes natürlicher Gewässer. Verhandlungen des Naturhistorisch– Medizinischen Vereins zu Heidelberg, Neue Folge 13: 395–481.

Lemmermann, E. (1900) Beiträge zur Kenntnis der Planktonalgen. X. Diagnosen neuer Schwebalgen. Berichte der deutsche botanischen Gesellschaft 18: 306–310.

Lin, S., Wu, Z.X., Yu, G.L., Zhu, M.L., Yu, B.S. & Li, R.H. (2010) Genetic diversity and molecular phylogeny of Planktothrix (Oscillatoriales, cyanobacteria) strains from China. Harmful Algae 9(1): 87–97.

http://dx.doi.org/10.1016/j.hal.2009.08.004

Meffert, M.E. (1988) Limnothrix Meffert nov. gen. The unsheathed planktic cyanophycean filaments with polar and central gas vacuoles. Algological Studies 50–53: 269–276.

Mischke, U. & Nixdorf, B. (2003) Equilibrium phase conditions in shallow German lakes: How Cyanoprokaryota species establish a steady state phase in late summer. Hydrobiologia 502: 123–132.

http://dx.doi.org/10.1007/978-94-017-2666-5_11

Mitchell, B.G. (1990) Algorithms for determining the absorption coefficient of aquatic particulates using the quantitative filter technique (QFT). In: Spinrad, R.W. (Ed.) Ocean Optics X, Proceedings-Society of Photo-Optical Instrumentation Engineers 1302: 137–148.

http://dx.doi.org/10.1117/12.21440

Neilan, B.A., Jacobs, D. & Goodman, A.E. (1995) Genetic diversity and phylogeny of toxic cyanobacteria determined by DNA polymorphisms within the phycocyanin locus. Applied Environmental Microbiology 61: 3327–3332.

Neilan, B.A., Jacobs, D.T., Del, Dot., Blackall, L.L., Hawkins, P.R., Cox, P.T. & Goodman, A.E. (1997) rRNA sequences and evolutionary relationships among toxic and nontoxic cyanobacteria of the genus Microcystis. International Journal of Systematic Bacteriolology 47: 693–697.

http://dx.doi.org/10.1099/00207713-47-3-693

Peterson, H.G., Hrudey, S.E., Cantin, I.A., Perley, T.R. & Kenefick, S.L. (1995) Physiological toxicity, cell membrane damage and the release of dissolved organic carbon and geosmin by Aphanizomenon flos-aquae after exposure to water treatment chemicals. Water Research 29(6): 1515–1523.

http://dx.doi.org/10.1016/0043-1354(94)00300-V

Posada, D. & Crandall, K.A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14(9): 817–818.

http://dx.doi.org/10.1093/bioinformatics/14.9.817

Rippka, R. (1988) Isolation and purification of cyanobacteria. Methods in Enzymology 167: 3–27.

http://dx.doi.org/10.1016/0076-6879(88)67004-2

Romo, S. & Miracle, M.R. (1994) Population dynamics and ecology of subdominant phytoplankton speciesin a shallow hypertrophic lake (Albufera of Valencia, Spain). Hydrobiologia 273: 31–56.

http://dx.doi.org/10.1007/BF00126767

Schwabe, G.H. (1964) Grundprobleme der Cyanophytentaxonomie. Gewässer und Abwässer 36: 7–39.

Shao, J.H., Xu, Y., Wang, Z.J., Jiang, Y.G., Yu, G.L., Peng, X. & Li, R.H. (2011) Elucidating the toxicity targets of β-ionone on photosynthetic system of Microcystis aeruginosa NIES-843 (Cyanobacteria). Aquatic Toxicology 104: 48–55.

http://dx.doi.org/10.1016/j.aquatox.2011.03.014

Stackebrandt, E. & Ebers, J. (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiology Today 33: 152–155.

Stackebrandt, E. & Goebel, B.M. (1994) A place for DNA–DNA reassociation and 16S ribosomal–RNA sequence–analysis in the present species definition in bacteriology. International Journal of Systematic and Evolutionary Microbiology 44: 846–849.

http://dx.doi.org/10.1099/00207713-44-4-846

Starmach, K. & Sieminska, J. (1966) Flora słodkowodna Polski, Volume 2. Polska Akademia Nauk Instytut Botaniki, Warsaw, Kraków, pp. 445–452.

Sthapit, E., Ochs, C.A. & Zimba, P.V. (2008) Spatial and temporal variation in phytoplankton community structure in a southeastern U.S. reservoir determined by HPLC and light microscopy. Hydrobiologia 600: 215–228.

http://dx.doi.org/10.1007/s10750-007-9234-7

Stomp, M., Huisman, J., de Jongh, F., Veraart, A.J., Gerla, D. & Rijkeboer, M. (2004) Adaptive divergence in pigment composition promotes phytoplankton biodiversity. Nature 432: 104–107.

http://dx.doi.org/10.1038/nature03044

Stomp, M., van Dijk, M.A., van Overzee, H.M.J., Wortel, M., Sigon, C.A.M. & Egas, M. (2008) The time scale of phenotypic plasticity, and its impact on competition in fluctuating environments. American Naturalist 172(5): 169–185.

http://dx.doi.org/10.1086/591680

Suda, S., Watanabe, M.M., Otsuka, S., Mahakahant, A., Yongmanitchai, W., Nopartnaraporn, N., Liu, Y.D. & Day, J.G.(2002) Taxonomic revision of water-bloom-forming species of oscillatorioid cyanobacteria. International Journal of Systematic and Evolutionary Microbiology 52: 1577–1595.

http://dx.doi.org/10.1099/ijs.0.01834-0

Szafer, W. (1910) Zur Kenntnis der Schwefelflora in der Umgebung von Lemberg. [Série B] Bulletin International de l’Académie des Sciences de Cracovie, Classe des Sciences Mathématiques et Naturelles 1910: 161–167.

Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution 30: 2725–2729.

http://dx.doi.org/10.1093/molbev/mst197

Taton, A., Grubisic, S., Brambilla, E., Rutger, D.V. & Wilmotte, A. (2003) Cyanobacterial diversity in natural and artificial microbial mats of Lake Fryxell (McMurado Dry Valleys, Antarctica): a morphological and molecular approach. Applied and Environment Microbiology 69: 5157–5169.

http://dx.doi.org/10.1128/AEM.69.9.5157-5169.2003

Tillett, D. & Neilan, B.A. (2000) Xanthogenate Nucleic Acid Isolation from Cultured and Environmental Cyanobacteria. Journal of Phycology 36: 251–258.

http://dx.doi.org/10.1046/j.1529-8817.2000.99079.x

Villena, M. & Romo, S. (2003) Phytoplankton changes in a shallow Mediterranean lake (Albufera of Valencia, Spain) after sewage diversion. Hydrobiologia 506–509: 281–287.

http://dx.doi.org/10.1023/B:HYDR.0000008565.23626.aa

Welsh, H. (1964) A contribution to our knowledge of the blue-green algae of South West Africa. Nova Hedwigia 7(1–2): 15–32.

Whitton, B.A. (2011) Cyanobacteria (Cyanophyta). In: John, D.M., Whitton, B.A. & Brook, A.J. (Eds.) The freshwater algal flora of the British Isles. An identification guide to freshwater and terrestrial algae. Cambridge University Press, Cambridge, pp. 31–158.

Zhu, M.L., Yu, G.L., Li, X.C., Tan, W.H. & Li, R.H. (2012) Taxonomic and phylogenetic evaluation of Limnothrix strains (Oscillatoriales, Cyanobacteria) by adding Limnothrix planktonica strains isolated from central China. Hydrobiologia 698(1): 367–374.

http://dx.doi.org/10.1007/s10750-012-1127-8


Refbacks

  • There are currently no refbacks.


ISSN 1179-3155 (print); ISSN 1179-3163 (online)

Published by Magnolia Press, Auckland, New Zealand