Abstract
A filamentous benthic cyanobacteria strain isolated from a tropical man-made pond in Malaysia was characterised using combined phenotypic and genetic approaches. Morphological and ultrastructural observations were performed together with growth measurements. Cell dimensions, thylakoid arrangement and apical cell shape with aerotopes were consistent with the description of Pseudanabaena amphigranulata (Goor) Anagnostidis. Molecular characterisation of the16S rRNA gene gave 94% pairwise sequence identity with Pseudanabaena sp. PCC 6802,which corresponds to the genus identification threshold value while also suggesting that the strain is distinctly different to the species of Pseudanabaena currently represented in available databases. The strain showed identical 16S-23S ITS configuration with other strains of Pseudanabaena apart from having a larger spacer region. Cultures of the strain were exposed to various temperature and photoperiod treatments and harvested at exponential phase in order to examine phenotypic plasticity. Significant relationships between environmental conditions and morphological characteristics (cell dimensions and shape) were identified for the first time within the genus Pseudanabaena. The maximum cell length (5.7 ± 0.07 μm) was observed at 25 °C under 12:12 light to dark, while the greatest cell width (3.2 ± 0.11 μm) was also observed at 25 °C but under 16:8 light to dark. The strain showed high plasticity in cell dimensions and shape under different temperature and photoperiod treatments, with25 °C under 12:12 light to dark providing the optimal conditions for its growth.





References
Acinas SG, Haverkamp TA, Huisman J, Stal LJ (2009) Phenotypic and genetic diversification of Pseudanabaena spp. (cyanobacteria). ISME J 3(1):31–46
Anagnostidis K (2001) Nomenclatural changes in cyanoprokaryotic order Oscillatoriales. Preslia 73:359–375
Andersen RA, Kawachi M (2005) Traditional microalgae isolation techniques. In: Anderson RA (ed) Algal culturing techniques. Elsevier, Amsterdam, pp 83-100.
Bertos-Fortis M, Farnelid HM, Lindh MV, Casini M, Andersson A, Pinhassi J, Legrand C (2016) Unscrambling cyanobacteria community dynamics related to environmental factors. Front Microbiol 7:625
Boyer SL, Flechtner VR, Johansen JR (2001) Is the 16S-23S rRNA internal transcribed spacer region a good tool for use in molecular systematics and population genetics? A case study in cyanobacteria. Mol Biol Evol 18:1057–1069
Bruno L, Billi D, Bellezza S, Albertano P (2009) Cytomorphological and genetic characterization of troglobitic Leptolyngbya strains isolated from Roman hypogea. Appl Environ Microbiol 75:608–617
Castenholz R W (2001) Phylum BX. Cyanobacteria. Oxygenic photosynthetic bacteria. In: Bergey’s manual of systematic bacteriology. Volume 1: the Archaea and the deeply branching and phototropic Bacteria. Springer, New York, pp. 413-439
Chen J, Banks D, Jarret RL, Jones JB (2000) Evidence for conserved tRNA genes in the 16S-23S rDNA spacer sequence and two rrn operons of Xylella fastidiosa. Can J Microbiol 46:1171–1175
Comte K, Sabacka M, Carre-Mlouka A, Elster J, Komárek J (2007) Relationships between the Arctic and the Antarctic cyanobacteria; three Phormidium–like strains evaluated by a polyphasic approach. FEMS Microbiol Ecol 59:366–376
Dehning I, Tilzer M (1989) Survival of Scenedesmus acuminatus (Chlorophyceae) in darkness. J Phycol 25:509–515
Emerson D, Agulto L, Liu H, Liu L (2008) Identifying and characterizing bacteria in an era of genomics and proteomics. Bioscience 58:925–936
Geitler L (1932) Cyanophyceae In: Rabenhorst, L. (Ed.) Kryptogamen Flora von Deutschland, Österreich und der Schweiz 14. Akademische Verlagsgesellschaft, Leipzig, pp. 130–159
van Goor ACJ (1918) Zur Kenntnis der Oscillatoriaceen. Reçueil des Travaux Botaniques Néerlandais 15:255–262
Graumann P, Marahiel MA (1996) Some like it cold: response of microorganisms to cold shock. Arch Microbiol 166:293–300
Gupta S, Agrawal SC (2006) Survival of blue-green and green algae under stress conditions. Folia Microbiol 51(2):121–128
Gugger M, Lyra C, Suominen I, Tsitko I, Humbert JF, Salkinoja-Salonen MS, Sivonen K (2002) Cellular fatty acids as chemotaxonomic markers of the genera Anabaena, Aphanizomenon, Microcystis, Nostoc and Planktothrix (cyanobacteria). Int J Syst Evol Microbiol 52:1007–1015
James F. Coles, R. Christian Jones, (2000) Effect of temperature on photosynthesis-light response and growth of four phytoplankton species isolated from a tidal freshwater river. J Phycol 36 :7-16
Kling H, Watson S (2003) A new planktic species of Pseudanabaena (Cyanoprokaryota, Oscillatoriales) from North American large lakes. Hydrobiologia 502:383–388
Komarek J (2003) Problem of the taxonomic category “species” in cyanobacteria. Algol Stud 109:281–297
Komárek J, Anagnostidis K (2005) Süsswasserflora von Mitteleuropa. Cyanoprokaryota: 2.Teil/2nd Part: Oscillatoriales. (Vol. 19): Elsevier Spektrum Akademischer Verlag, Munich, pp.86
Komarek J, Kastovsky J, Mares J, Johansen RJ (2014) Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) 2014, using a polyphasic approach. Preslia 86:295–335
Lauterborn R (1915) Die sapropelische Lebewelt. Ein Beitragzur Biologie des Faulschlammesnatürlicher Gewässer. Verhs Naturhist Med Vereins Heidelberg. Neue Folge 13:395–481
Lyra C, Suomalainen S, Gugger M, Vezie C, Sundman P, Paulin L, Sivonen K (2001) Molecular characterization of planktic cyanobacteria of Anabaena, Aphanizomenon, Microcystis and Planktothrixgenera. Int J Syst Evol Microbiol 51:513–526
Marquardt J, Palinska KA (2007) Genotypic and phenotypic diversity of cyanobacteria assigned to the genus Phormidium (Oscillatoriales) from different habitats and geographical sites. Arch Microbiol 187:397–413
Montagnes DS, Franklin DJ (2001) Effect of temperature on diatom volume, growth rate, and carbon and nitrogen content: reconsidering some paradigms. Limnol Oceanogr 46:2008–2018
Oufdou K, Mezrioui N, Oudra B, Loudiki M, Barakate M, Sbiyyaa B (2001) Bioactive compounds from Pseudanabaena species (cyanobacteria). Microbios 106(Suppl 1):21–29
Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61
Ronquist F, Huelsenbeck JP (2003) MRBAYES 3—Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Salih S, Alkarkhi A, Lalung J, Ismail N (2013) Water quality of river, lake and drinking water supply in Penang State by means of multivariate analysis. World Appl Sci J 26:75–82
Schwabe GH (1964) Grundprobleme der Cyanophytentaxonomie. Gewässer und Abwässer 36:7–39
Sciuto K, Andreoli C, Rascio N, La Rocca N, Moro I (2012) Polyphasic approach and typification of selected Phormidium strains (cyanobacteria). Cladistics 28:357–374
Singh SP, Singh P (2015) Effect of temperature and light on the growth of algae species: a review. Renew Sust Energy Rev 50:431–444
Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33:152–155
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6, molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Tyystjarvi E, Aro EM (1996) The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Plant Biol 93:2213–2218
Whitton B A (2011) Cyanobacteria (Cyanophyta) In: John, D.M., Whitton, B.A. and 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
Winder M, Sommer U (2012) Phytoplankton response to a changing climate. Hydrobiologia 698:5–16
Yu G, Zhu M, Chen Y, Pan Q, Chai W, Li R (2015) Polyphasic characterization of four species of Pseudanabaena (Oscillatoriales,Cyanobacteria) from China and insights into polyphyletic divergence within the Pseudanabaena genus. Phytotaxa 192:1–12
Zapomelova E, Hisem D, Rehakova K, Hrouzek P, Jezberova J, Komarkova J, Korelusova J, Znachor P (2008) Experimental comparison of phenotypic plasticity and growth (cyanobacteria). J Plankton Res 30:1257–1269
Acknowledgements
We thank Mohammed BasriEshak for assistance with statistical analysis.
Funding
This study was funded and supported by Flagship grant (304/PBIOLOGI/650723/P131) under Ministry of Science, Technology and Innovation, Malaysia. P. Convey is supported by NERC core funding to the BAS ‘Biodiversity, Evolution and Adaptation’ Team.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Khan, Z., Wan Omar, W., Mohd Sidik Merican, F. et al. Characterisation of Pseudanabaena amphigranulata (Synechococcales) isolated from a man-made pond, Malaysia: a polyphasic approach. J Appl Phycol 30, 3187–3196 (2018). https://doi.org/10.1007/s10811-018-1392-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-018-1392-7