Abstract
Porphyrosiphon annulatus sp. nov. belonging to Microcoleaceae, Oscillatoriales was collected from the moist soil under the rock in the Gwanggyo Mountain of Suwon City, Gyeonggi Province, Korea and cultured. Using the raw and cultured samples of the collected strains, we observed their morphological features through LM and TEM. Furthermore, their 16S rRNA gene and 16S–23S rRNA intergenic transcribed spacer (ITS) sequences were determined to be used phylogenetic analyses. We affirmed that thick sheath of the cells possessed transversely annular and longitudinal lamellations. The ultrastructure of thylakoids was a radial arrangement, which corresponds with a characteristic of the Microcoleaceae. In addition, P. annulatus displays the most similar morphology with type species P. notarisii; however, it differently holds the transversely annular lamellations with a shorter cell length and relatively dense trichome. Our 16S rRNA gene phylogeny showed that P. annulatus formed a clade with P. notarisii, and their DNA similarity was calculated to be 96.2%. The family Microcoleaceae was found to be paraphyletic with a distinct linage of the genus Porphyrosiphon. The ITS sequence of P. annulatus was unique in length and nucleotide composition, with different secondary structures of D1–D1ʹ and Box-B helices compared to those of close relatives. Overall, morphology and genetic traits of the Korean Porphyrosiphon suggest that P. annulatus should be considered to be a novel species.
References
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Komárek, J. & Anagnostidis, K. (2005) Cyanoprokaryota. 2. Teil: Oscillatoriales. In: Büdel, B., Krienitz, L., Gärtner, G. & Schagerl, M. (Eds.) Sü?wasserflora von Mitteleuropa, Vol. 19/2. Elsevier, Spektrum, Heidelberg, pp. 1–759.
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Lee, N-J., Seo, Y., Ki, J.-S. & Lee, O.-M. (2020) Morphology and molecular description of Wilmottia koreana sp. nov. (Oscillatoriales, Cyanobacteria) isolated from the Republic of Korea. Phytotaxa 447: 237–251. https://doi.org/10.11646/phytotaxa.447.4.2
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Page, R.D.M. (1996) TreeView: an application to display of phylogenetic trees on personal computers. Computer Applications in the Biosciences 12: 357–358. https://doi.org/10.1093/bioinformatics/12.4.357
Richards, E., Reichardt, M. & Rogers, S. (2003) Preparation of genomic DNA from plant tissue. In: Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. & Struhl, K. (Eds.) Current protocols in molecular biology. John Wiley and Sons, Inc., New York, pp. 2.3.1–2.3.7.
Rippka, R., Waterbury, J. & Cohen-Bazire, G. (1974) A cyanobacterium which lacks thylakoids. Archives of Microbiology 100: 419–436. https://doi.org/10.1007/BF00446333
Rippka, R., Deruelles, J., Waterbury, J.B., Herdman, M. & Stanier, R.Y. (1979) Generic assignments, strain histories and properties of pure cultures of Cyanobacteria. Journal of General Microbiology 111: 1–61. https://doi.org/10.1099/00221287-111-1-1
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Shariatmadari, Z., Moharrek, F., Riahi, H., Heidari, F. & Aslani, E. (2017) Efficiency of partial 16S rRNA gene sequencing as molecular marker for phylogenetic study of cyanobacteria, with emphasis on some complex taxa. Acta Biologica Szegediensis 61: 59–68.
Siegesmund, M.A., Johansen, J.R., Karsten, U. & Friedl, T. (2008) Coleofasciculus gen. nov. (Cyanobacteria): morphological and molecular criteria for revision of the genus Microcoleus Gomont. Journal of Phycology 44: 1572–1585. https://doi.org/10.1111/j.1529-8817.2008.00604.x
Strunecký, O., Bohunická, M., Johansen, J.R., ?apková, K., Raabová, L., Dvo?ák, P. & Komárek, J. (2017) A revision of the genus Geitlerinema and a description of the genus Anagnostidinema gen. nov. (Oscillatoriophycidae, Cyanobacteria). Fottea 17: 114–126. https://doi.org/10.5507/fot.2016.025
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Strunecký, O., Komárek, J. & Šmarda, J. (2014) Kamptonema (Microcoleaceae, Cyanobacteria), a new genus derived from the polyphyletic Phormidium on the basis of combined molecular and cytomorphological markers. Preslia 86: 193–207.
Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research 31: 3406–3415. https://doi.org/10.1093/nar/gkg595
Anagnostidis, K. (1989) Geitlerinema, a new genus of oscillatorialean cyanophytes. Plant Systematics and Evolution 164: 33–46. https://dx.doi.org/10.1007/BF00940428
Anagnostidis, K. & Komárek, J. (1988) Modern approach to the classification system of cyanophytes. 3. Oscillatoriales. Archiv für Hydrobiologie, Supplement 80: 327–472.
Baker, A.F. & Bold, H.C. (1970) Phycological Studies. X. Taxonomic studies in the Oscillatoriaceae. University of Texas Publication 7004: 1–105.
Becerra-Absalón, I., Muñoz-Martín, M., Montejano, G. & Mateo, P. (2019) Differences in the cyanobacterial community composition of biocrusts from the drylands of Central Mexico. Are there endemic species? Frontiers in Microbiology 10: 1–21. https://doi.org/10.3389/fmicb.2019.00937
Casamatta, D.A., Vis, M.L. & Sheath, R.G. (2003) Cryptic species in cyanobacterial systematics: a case study of Phormidium retzii (Oscillatoriales) using 16S rDNA and RAPD analyses. Aquatic Botany 77: 295–309. https://doi.org/10.1016/j.aquabot.2003.08.005
Casamatta, D., Stani?, D., Gantar, M. & Richardson, L.L. (2012) Characterization of Roseofilum reptotaenium (Oscillatoriales, Cyanobacteria) gen. et sp. nov. isolated from Caribbean black band disease. Phycologia 51: 489–499. https://doi.org/10.2216/11-10.1
De Toni, G.B. (1892) Sylloge algarum omnium hucusque cognitarum. Vol. 2. Bacillarieae; sectio II. Pseudoraphideae. Typis Seminarrii, Patavii, pp. 491–817
Drouet, F. (1937) The Brazilian Myxophyceae. I. American Journal of Botany 24: 598–608.
Dvo?ák, P., Jahodá?ová, E., Hašler, P., Gusev, E. & Poulí?ková, A. (2015) A new tropical cyanobacterium Pinocchia polymorpha gen. et sp. nov. derived from the genus Pseudanabaena. Fottea 15: 113–120. https://doi.org/10.5507/fot.2015.010
Fritsch, F.E. & Rich, F. (1924) Contributions to our knowledge of the freshwater Algae of Africa. 4. Freshwater and subaerial algae from Natal. Transactions of the Royal Society of South Africa 11: 297–398.
Gardner, N.L. (1927) New Myxophyceae from Porto Rico. Memoirs of the New York Botanical Garden 7: 1–144, pls. 1–23.
Geitler, L. (1932) Cyanophycceae. In: Rabenhorst, L. (Ed.) Kryptogamen-Flora von Deutschland, Österreich und der Schweiz. Vol. 14. Akademische Verlagsgesellschaft, Leipzig, pp. 1–1196.
Gomont, M. (1892) Monographie des Oscillariées (Nostocacées Homocystées). Deuxième partie. -Lyngbyées. Annales des Sciences Naturelles, Botanique, Série 7 15: 263–368; 16: 91–264.
Genuário, D.B., Vieira Vaz, M.G.M., Hentschke, G.S., Sant’Anna, C.L. & Fiore, M.F. (2015) Halotia gen. nov., a phylogenetically and physiologically coherent cyanobacterial genus isolated from marine coastal environments. International Journal of Systematic and Evolutionary Microbiology 65: 663–675. https://doi.org/10.1099/ijs.0.070078-0
Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59: 307–321. https://doi.org/10.1093/sysbio/syq010
Guiry, M.D. & Guiry, G.M. (2021) AlgaeBase. World-wide electronic publication. National University of Ireland, Galway. Available from: http://www.algaebase.org/ (accessed 1 April 2021).
Hašler, P., Dvo?ák, P., Johansen, J.R., Kitner, M., Ond?ej, V. & Poulí?ková, A. (2012) Morphological and molecular study of epipelic filamentous genera Phormidium, Microcoleus and Geitlerinema (Oscillatoriales, Cyanophyta/Cyanobacteria). Fottea 12: 341–356. https://doi.org/10.5507/fot.2012.024
Hrouzek, P., Lukešová, A., Mareš, J. & Ventura, S. (2013) Description of the cyanobacterial genus Desmonostoc gen. nov. including D. muscorum comb. nov. as a distinct, phylogenetically coherent taxon related to the genus Nostoc. Fottea 13: 201–213. https://doi.org/10.5507/fot.2013.016
Jaag, O. (1945) Untersuchungen über die Vegetation und Biologie der Algen des nackten Gesteins in den Alpen, im Jura und im schweizerischen Mittelland. Beiträge zur Kryptogamenflora der Schweiz (Bern) 9: 1–560.
Kaštovský, J., Veselá, J., Bohunická, M., Fu?íková, K., Štenclová, L. & Brewer-Carias, C. (2016) New and unusual species of cyanobacteria, diatoms and green algae, with a description of a new genus Ekerewekia gen. nov. (Chlorophyta) from the table mountain Churí-tepui, Chimantá Massif (Venezuela). Phytotaxa 247: 153–180. https://dx.doi.org/10.11646/phytotaxa.247.3.1
Katoh, K. & Stanley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. https://doi.org/10.1093/molbev/mst010
Kiel, G. & Gaylarde, C.C. (2006) Bacterial diversity in biofilms on external surfaces of historic buildings in Porto Alegre. World Journal of Microbiology and Biotechnology 22: 293–297. https://doi.org/10.1007/s11274-005-9035-y
Kim, J.-H., Jeong, M.S., Kim, D.-Y., Her, S. & Wie, M.-B. (2015) Zinc oxide nanoparticles induce lipoxygenase-mediated apoptosis and necrosis in human neuroblastoma SH-SY5Y cells. Neurochemistry International 90: 204–214. https://doi.org/10.1016/j.neuint.2015.09.002
Kim, M., Oh, H.-S., Park, S.-C. & Chun, J. (2014) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. International Journal of Systematic and Evolutionary Microbiology 64: 346–351. https://doi.org/10.1099/ijs.0.059774-0
Kirchner, O. (1898) Schizophyceae. In: Engler, A. & Prantl, K. (Eds.) Die natürlichen Pflanzenfamilien, 1. Teil, Abteilung a. Wilhelm Engelmann, Leipzig, pp. 45–92.
Komárek, J. (2016) A polyphasic approach for the taxonomy of cyanobacteria: principles and applications. European Journal of Phycology 51: 346–353. https://doi.org/10.1080/09670262.2016.1163738
Komárek, J. & Anagnostidis, K. (2005) Cyanoprokaryota. 2. Teil: Oscillatoriales. In: Büdel, B., Krienitz, L., Gärtner, G. & Schagerl, M. (Eds.) Sü?wasserflora von Mitteleuropa, Vol. 19/2. Elsevier, Spektrum, Heidelberg, pp. 1–759.
Komárek, J., Kaštovský, J., Mareš, J. & Johansen, J.R. (2014) Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) 2014, using a polyphasic approach. Preslia 86: 295–335.
Komárek, J., Zapom?lová, E., Šmarda, J., Kopecký, J., Rejmánková, E., Woodhouse, J., Neilan, B.A. & Komárková, J. (2013) Polyphasic evaluation of Limnoraphis robusta, a water-bloom forming cyanobacterium from Lake Atitlán, Guatemala, with a description of Limnoraphis gen. nov. Fottea 13: 39–52. https://doi.org/10.5507/fot.2013.004
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
Lee, N-J., Seo, Y., Ki, J.-S. & Lee, O.-M. (2019) A study of newly recorded genus and species for aerial cyanobacteria Wilmottia murrayi (Oscillatoriales, Cyanobacteria) in Korea. Korean Journal of Environmental Biology 37: 260–267. https://doi.org/10.11626/KJEB.2019.37.3.260
Lee, N-J., Seo, Y., Ki, J.-S. & Lee, O.-M. (2020) Morphology and molecular description of Wilmottia koreana sp. nov. (Oscillatoriales, Cyanobacteria) isolated from the Republic of Korea. Phytotaxa 447: 237–251. https://doi.org/10.11646/phytotaxa.447.4.2
Nguyen, L.T.T. Cronberg, G. Moestrup, O. & Daugbjerg, N. (2013) Annamia toxica gen. et sp. nov.(Cyanobacteria), a freshwater cyanobacterium from Vietnam that produces microcystins: ultrastructure, toxicity and molecular phylogenetics. Phycologia 52: 25–36. https://doi.org/10.2216/10-097.1
Nowicka-Krawczyk, P., Mühlsteinová, R. & Hauer, T. (2019) Detailed characterization of the Arthrospira type species separating commercially grown taxa into the new genus Limnospira (Cyanobacteria). Scientific Reports 9: 1–11. https://doi.org/10.1038/s41598-018-36831-0
Page, R.D.M. (1996) TreeView: an application to display of phylogenetic trees on personal computers. Computer Applications in the Biosciences 12: 357–358. https://doi.org/10.1093/bioinformatics/12.4.357
Richards, E., Reichardt, M. & Rogers, S. (2003) Preparation of genomic DNA from plant tissue. In: Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. & Struhl, K. (Eds.) Current protocols in molecular biology. John Wiley and Sons, Inc., New York, pp. 2.3.1–2.3.7.
Rippka, R., Waterbury, J. & Cohen-Bazire, G. (1974) A cyanobacterium which lacks thylakoids. Archives of Microbiology 100: 419–436. https://doi.org/10.1007/BF00446333
Rippka, R., Deruelles, J., Waterbury, J.B., Herdman, M. & Stanier, R.Y. (1979) Generic assignments, strain histories and properties of pure cultures of Cyanobacteria. Journal of General Microbiology 111: 1–61. https://doi.org/10.1099/00221287-111-1-1
Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D.L., Darling, A., Höhna, 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
Shariatmadari, Z., Moharrek, F., Riahi, H., Heidari, F. & Aslani, E. (2017) Efficiency of partial 16S rRNA gene sequencing as molecular marker for phylogenetic study of cyanobacteria, with emphasis on some complex taxa. Acta Biologica Szegediensis 61: 59–68.
Siegesmund, M.A., Johansen, J.R., Karsten, U. & Friedl, T. (2008) Coleofasciculus gen. nov. (Cyanobacteria): morphological and molecular criteria for revision of the genus Microcoleus Gomont. Journal of Phycology 44: 1572–1585. https://doi.org/10.1111/j.1529-8817.2008.00604.x
Strunecký, O., Bohunická, M., Johansen, J.R., ?apková, K., Raabová, L., Dvo?ák, P. & Komárek, J. (2017) A revision of the genus Geitlerinema and a description of the genus Anagnostidinema gen. nov. (Oscillatoriophycidae, Cyanobacteria). Fottea 17: 114–126. https://doi.org/10.5507/fot.2016.025
Strunecký, O., Elster, J. & Komárek, J. (2011) Taxonomic revision of the freshwater cyanobacterium “Phormidium” murrayi = Wilmottia murrayi. Fottea 11: 57–71. https://doi.org/10.5507/fot.2011.007
Strunecký, O., Komárek, J. & Šmarda, J. (2014) Kamptonema (Microcoleaceae, Cyanobacteria), a new genus derived from the polyphyletic Phormidium on the basis of combined molecular and cytomorphological markers. Preslia 86: 193–207.
Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research 31: 3406–3415. https://doi.org/10.1093/nar/gkg595