Fottea 2022, 22(1):78-92 | DOI: 10.5507/fot.2021.017

Geosmin-producing Scytonema foetidum sp. nov. (Scytonemataceae, Cyanobacteria): morphology and molecular phylogeny

Wittaya Tawong1, 2*, Pongsanat Pongcharoen1, 2, Tomohiro Nishimura3
1 Department of Agricultural Science, Faculty of Agricultural Natural Resources and Environment, Naresuan University, Phitsanulok 65000, Thailand; *Corresponding author e-mail: wittayat@nu.ac.th
2 Center of Excellence in Research in Agricultural Biotechnology, Naresuan University, Phitsanulok 65000, Thailand
3 Cawthron Institute, Nelson 7010, New Zealand

A novel Scytonema species, Scytonema foetidum sp. nov. is described by combining morphological and genetic evidences. Two clonal strains of the new species were isolated from a wet soil sample taken from the Khek River in the lower northern part of Thailand. This species is morphologically similar to S. hofmanii, but can be differentiated by a small filament width, conically rounded apical cell, and sheath present throughout the whole trichome. The 16S ribosomal RNA (rRNA), rbcLX, and nifH phylogenetic trees indicated that S. foetidum clearly formed a unique cluster within the Scytonema sensu stricto clade and shared low 16S rRNA sequence similarity (<98.4%) with the phylogenetically related taxa, supporting separation at species level. The 16S-23S rRNA internal transcribed spacer (ITS) sequences of S. foetidum also possessed unique secondary structures in D1-D1', Box B, and V3 helices, differentiating this species from other known Scytonema species. Furthermore, S. foetidum could produce the odoriferous compound, geosmin.

Keywords: Cyanobacteria, Geosmin, 16S rRNA phylogeny, ITS secondary structure, Scytonema, Systematics, Taxonomy, Thailand

Received: May 28, 2021; Revised: August 4, 2021; Accepted: September 17, 2021; Prepublished online: January 10, 2022; Published: April 1, 2022  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Tawong, W., Pongcharoen, P., & Nishimura, T. (2022). Geosmin-producing Scytonema foetidum sp. nov. (Scytonemataceae, Cyanobacteria): morphology and molecular phylogeny. Fottea22(1), 78-92. doi: 10.5507/fot.2021.017
Download citation

Attachments

Download fileFot_2022_1_78-92_suppl.pdf

File size: 2.49 MB

References

  1. Bornet, É. & Flahault, C. (1888): Revision des Nostocacées hétérocystées contenues dans les principaux herbiers de France (quatrième et dernier fragment). Annales des Sciences Naturelles. - Botanique,Septième Série 7: 177-262.
  2. Berthold, D.E.; Lefler, F.W.; Huang, I-S.; Abdulla, H.; Zimba, P.V. & Laughinghouse IV, H.D. (2021): Iningainema tapete sp. nov. (Scytonemataceae, Cyanobacteria) from greenhouses in central Florida (USA) produces two types of nodularin with biosynthetic potential for microcystin-LR and anabaenopeptin production. - Harmful Algae 101: 101969. Go to original source...
  3. Cai, F.F.; Yang, Y.; Wen, Q. & Li, R. (2018): Desmonostoc danxiaense sp. nov. (Nostocales, Cyanobacteria) from Danxia mountain in China based on polyphasic approach. - Phytotaxa 367: 233-244. Go to original source...
  4. Casamatta, D.A. & Vis, M.L. (2004): Current velocity and nutrient level effects on the morphology of Phormidium retzii (Cyanobacteria) in artificial stream mesocosms. - Algological Studies 113:87-99. Go to original source...
  5. Catherine, Q.; Susanna, W.; Isidora, E-S.; Mark, H.; Aurélie, V. & Jean-François, H. (2013): A review of current knowledge on toxic benthic freshwater cyanobacteria - Ecology, toxin production and risk management. - Water Research 47: 5464-5479. Go to original source...
  6. Choi, H.J.; Joo, J-H.; Kim, J-H.; Wang, P.; Ki, J-S. & Han, M-S. (2018): Morphological characterization and molecular phylogenetic analysis of Dolichospermum hangangense (Nostocales, Cyanobacteria) sp. nov. from Han River, Korea. - Algae 33: 143-156. Go to original source...
  7. Churro, C.; Semedo-Aguiar, A.P.; Silva, A.D.; Pereira-Leal, J.B. & Leite, R.B. (2020): A novel cyanobacterial geosmin producer, revising GeoA distribution and dispersion patterns in Bacteria. - Scientific Reports 10: 8679. Go to original source...
  8. Correns, C. (1889): Ueber Dickenwachsthum durch Intussusception bei einigen Algenmembranen. - Flora (Jena) 72: 298-347.
  9. Edgar, R.C. (2004): MUSCLE: multiple sequences alignment with high accuracy and high throughput. - Nucleic Acids Research 32: 1792-1797. Go to original source...
  10. Erwin, P. & Thacker, R.W. (2008): Cryptic diversity of the symbiotic cyanobacterium Synechococcus spongiarum among sponge hosts. - Molecular Ecology 17: 2937-2947. Go to original source...
  11. Fiore, M.F.; Sant'Anna, C.L.; Azevedo, M.T.P.; Komárek, J.; Kaštovský, J.; Sulek, J. & Lorenzi, A.S. (2007): The cyanobacterial genus Brasilonema molecular and phenotype evaluation. - Journal of Phycology 43: 789-798. Go to original source...
  12. Godo, T.; Saki, Y.; Nojiri, Y.; Tsujitani, M.; Sugahara, S.; Hayashi, S.; Kamiya, H.; Ohtani, S. & Seike, Y. (2017): Geosmin-producing Species of Coelosphaerium (Synechococcales, Cyanobacteria) in Lake Shinji. Japan. Scientific Reports 7: 41928. Go to original source...
  13. 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. Go to original source...
  14. Hašler, P.; Dvořák, P.; Poulíčková, A. & Casamatta, D.A. (2014): A novel genus Ammassolinea gen.nov. (Cyanobacteria) isolate from subtropical epipelic habitats. - Fottea 14: 241-248. Go to original source...
  15. Hayashi, S.; Ohtani, S.; Godo, T.; Nojiri, Y.; Saki, Y.; Esumi, T. & Kamiya, H. (2019): Identification of geosmin biosynthetic gene in geosmin-producing colonial cyanobacteria Coelosphaerium sp. and isolation of geosmin non-producing Coelosphaerium sp. from brackish Lake Shinji in Japan. - Harmful Algae 84: 19-26. Go to original source...
  16. Hentschke, G.S. & Komárek, J. (2014): Scytonema santannae, a new morphospecies of cyanobacteria from the Atlantic rainforest, southeastern Brazil. - Brazilian Journal of Botany 37: 293-298. Go to original source...
  17. Johansen, J.R. & Casamatta, D.A. (2005): Recognizing cyanobacterial diversity through adoption of a new species paradigm. - Algological Studies (Cyanobacterial Research 6) 117: 71-93. Go to original source...
  18. Johansen, J.R.; Kovacik, L.; Casamatta, D.A.; Iková, K.F. & Kaštovský, J. (2011): Utility of 16S-23S ITS sequence and secondary structure for recognition of intrageneric and intergeneric limits within cyanobacterial taxa: Leptolyngbya corticola sp. nov. (Pseudanabaenaceae, Cyanobacteria). - Nova Hedwigia 92: 283-302. Go to original source...
  19. Johansen, J.R.; Mareš, J.; Pietrasiak, N.; Bohunická, M.; Zima Jr., J.; Štenclová, L. & Hauer, T. (2017): Highly divergent 16S rRNA sequences in ribosomal operons of Scytonema hyalinum (Cyanobacteria). - PLoS One 12: e0186393. Go to original source...
  20. Kim, K.; Park, C.; Yoon, Y. & Hwang, S.J. (2018): Harmful cyanobacterial material production in the North Han River (South Korea): Genetic potential and temperature dependent properties. - International Journal of Environmental Research and Public Health 15: 444. Go to original source...
  21. 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. Go to original source...
  22. Kiseleva, E. (1930): About a new bluegreen algae Scytonematopsis woronichinii. - Zhurnal Russkago Botanicheskago Obshchestva pri Akademii Nauk. 15: 169-174.
  23. Komárek, J. (2013): Cyanoprokaryota. 3. Teil / 3rd part: Heterocytous Genera. - In: Ettl, H., Gerloff J., Heynig, H. & Pascher, A. (eds): Süßwasserflravon Mitteleuropa, Bd. 19/3. - 1130 pp., Springer, Berlin.
  24. Komárek, J. & Johansen, J. (2015): Filamentous cyanobacteria. - In: Wehr, J.D., Sheath, R.G. & Kociolek, J.P. (eds): Freshwater algae of North America. Ecology and classification. - pp. 135-235, Academic Press, San Diego. Go to original source...
  25. Komárek, J.; Sant'Anna, C.L.; Bohunická, M.; Mareš, J.; Hentschke, G.S.; Rigonato, J. & Fiore, M.F. (2013): Phenotype diversity and phylogeny of selected Scytonema-species (Cyanoprokaryota) from SE Brazil. - Fottea 13:173-200. Go to original source...
  26. 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.
  27. Komárková, J.; Zapomĕlová, E. & Komárek, J. (2013): Chakia (cyanobacteria), a new heterocytous genus from Belizean marshes identified on the basis of the 16S rRNA gene. - Fottea 13: 227-233. Go to original source...
  28. 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. Go to original source...
  29. Lowe, T.M. & Eddy, S.R. (1997): tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. - Nucleic Acids Research 25: 955-964. Go to original source...
  30. Mai, T.; Johansen, J.R.; Pietrasiak, N.; Bohunická, M. & Martin, P.M. (2018): Revision of the Synechococcales (Cyanobacteria) through recognition of four families including Oculatellaceae fam. nov. and Trichocoleaceae fam. nov. and six new genera containing 14 species. - Phytotaxa 365: 001-059. Go to original source...
  31. Mareš, J. (2018): Multilocus and SSU rRNA gene phylogenetic analyses of available cyanobacterial genomes, and their relation to the current taxonomic system. - Hydrobiologia 811: 19-34. Go to original source...
  32. Mathews Lab, University of Rochester Medical Center. (2018): RNA structure, version 6.0.1 - Available from: https://rna.urmc.rochester.edu/RNAstructure.html (accessed 16 April 2018)
  33. McGregor, G.B. (2018): Freshwater cyanobacteria of north-eastern Australia: 3. Nostocales. - Phytotaxa 359: 1-166. Go to original source...
  34. McGregor, G.B. & Sendall, B.C. (2017a): Iningainerma pulvinus gen nov., sp nov. (Cyanobacteria, Scytonemataceae) a new nodularin producer from Edgbaston Reserve, north-eastern Australia. - Harmful Algae 62: 10-19. Go to original source...
  35. McGregor, G.B. & Sendall, B.C. (2017b): Ewamiania thermalis gen. et sp. nov. (Cyanobacteria, Scytonemataceae), a new cyanobacterium from Talaroo thermal springs, north-eastern Australia. - Australian Systematic Botany 30: 38-47. Go to original source...
  36. McGregor, G.B. & Sendall, B.C. (2021): True branching and phenotypic plasticity in the planktonic cyanobacterium Dolichospremum branchiatum sp. nov. (Nostocales, Aphanizomenonaceae), from south-eastern Australia. - Phytotaxa 491: 093-114. Go to original source...
  37. Nylander, J.A.A. (2004): MrModeltest v2. Program distributed by the author. - Evolutionary Biology Centre, Uppsala University.
  38. Okonechnikov, K.; Golosova, O.; Fursov, M. & UGENE team. (2012): Unipro UGENE: a unified bioinformatics toolkit. - Bioinfromatics 28: 1166-1167. Go to original source...
  39. Olson, J.B.; Steppe, T.F.; Litaker, R.W.& Paerl, H.W. (1998): N2-fixing microbial consortia associated with the ice cover of Lake Bonney, Antarctica. - Microbial Ecology 36: 231-238. Go to original source...
  40. Osorio-Santos, K.; Pietrasiak, N.; Bohunická, M.; Miscoe, L.H.; Kováčik, L.; Martin, M.P. & Johansen, J.R. (2014): Seven new species of Oculatella (Pseudanabaenales, Cyanobacteria): taxonomically recognizing cryptic diversification. - European Journal of Phycology 49: 450-470. Go to original source...
  41. Palinska, K.A. & Surosz, W. (2014): Taxonomy of cyanobacteria: a contribution to consensus approach. - Hydrobiologia 740: 1-11. Go to original source...
  42. Perkerson, R.B. III; Johansen, J.R.; Kováčik, L.; Brand, J.; Kaštovský, J. & Casamatta, D.A. (2011): A unique pseudanabaenalean (cyanobacteria) genus Nodosilinea gen. nov. based on morphological and molecular data. - Journal of Phycology 47: 1397-1412. Go to original source...
  43. Pietrasiak, N.; Reeve, S.; Osorio-Santos, K.; Lipson, D.A. & Johansen, J.R. (2021): Trichotorquatus gen. nov. - A new genus of soil cyanobacteria discovered from American drylands. - Journal of Phycology: In press. Go to original source...
  44. Sant'Anna, C.L.; Azevedo, T.M.P.; Kaštovský, J. & Komárek, J. (2010): Two form-genera of aerophytic heterocytous cyanobacteria from Brasilian rainy forest "Mata Atlântica". - Fottea 10:217-228. Go to original source...
  45. Saraf, A.; Dawda, H.G.; Suradkar, A.; Batule, P.; Behere, I.; Kotulkar, M.; Kumat, A. & Singh, P. (2018): Insights into the phylogeny of false-branching heterocytous cyanobacteria with the description of Scytonema pachmarhiense sp. nov. isolated from Pachmarhi Biosphere Reserve, India. - FEMS Microbiology Letters 365: 1-9. Go to original source...
  46. Singh, P.; Minz, R.; Kunui, K.; Shaikh, Z.M.; Suradkar, A.; Shouche, Y.S.; Mishra, A.K. & Singh, S.S. (2017): A new species of Scytonema isolated from Bilaspur, Chhattisgarh, India using the polyphasic approach. - Plant Systematics and Evolution volume 303: 249-258 Go to original source...
  47. Singh, P.; Minj, R.A.; Kunui, K.; Shaikh, M.Z.; Suradkar, A.; Shouche, Y.S.; Mishra, A.K. & Singh, S.S. (2016): A new species of Scytonema isolated from Bilaspur, Chhattisgarh, India. - Journal of Systematics and Evolution 9999: 1-9 Go to original source...
  48. Sendall, B.C. & McGregor, G.B. (2018): Cryptic diversity within the Scytonema complex: Characterization of paralytic shellfish toxin producer Herteroscytonema crispum, and the establishment of the family Heteroscytonemataceae (Cyanobacteria/Nostocales). - Harmful Algae 80: 158-170. Go to original source...
  49. Stackebrandt, E. & Ebers, J. (2006): Taxonomic parameters revisited: tarnished gold standards. - Microbiology Today 4: 152-155.
  50. Suurnäkki, S.; Gomez-Saez, G.V.; Rantala-Ylinen, A.; Jokela, J., Fewer, D.P. & Sivonen, K. (2015): Identification of geosmin and 2-methylisoborneol in cyanobacteria and molecular detection methods for the producers of these compounds. - Water Research 68: 56-66. Go to original source...
  51. Tanabe, Y.; Kasai, F. &Watanabe, M. M. (2007): Multilocus sequence typing (MLST) reveals high genetic diversity and clonal population structure of the toxic cyanobacterium Microcystis aeruginosa. - Microbiology 153: 3695-3703. Go to original source...
  52. Tawong, W. (2017): Diversity of the potential 2-Methylisoborneol-producing genotypes in Thai strains of Planktothricoides (Cyanobacteria). - Brazilian Archives of Biology and Technology 60: e17160567. Go to original source...
  53. Tawong, W.; Pongcharoen, P.; Pongpadung, P. & Ponza, P. (2019): Neowollea manoromense gen. & sp. nov. (Nostocales, Cyanobacteria), a novel geosmin producer isolated from Thailand. - Phytotaxa 424: 1-17. Go to original source...
  54. Rajaniemi, P.; Hrouzek, P.; Kastovska, K.; Willame, R.; Rantala, A.; Hoffmann, L.; Komárek, J. & Sivonen, K. (2005): Phylogenetic and morphological evaluation of the genera Anabaena, Aphanizomenon, Trichormus and Nostoc (Nostocales, Cyanobacteria). - International Journal of Systematic and Evolutionary Microbiology 55: 11-26. Go to original source...
  55. 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. Go to original source...
  56. Rudi, K.; Skulberg, M.O. & Jakobsen K.S. (1998): Evolution of cyanobacteria by exchange of genetic material among phylogenetically related strains. - Journal of Bacteriology 180: 3453-3461. Go to original source...
  57. Wang, Z.; Song, G.; Li, Y.; Yu, G.; Hou, X.; Gan, Z. & Li, R. (2019): The diversity, origin, and evolutionary analysis of geosmin synthase in cyanobacteria. - Science of the Total Environment 689: 789-796. Go to original source...
  58. Willame, R.; Boutte, C.; Grubisic, S.; Wilmotte, A.; Komárek, J. & Hoffmann, L. (2006): Morphological and molecular characterization of planktonic cyanobacteria from Belgium and Luxembourg. - Journal of Phycology 42: 1312-1332. Go to original source...
  59. Willis, A. & Woodhouse, J.N. (2020): Defining cyanobacterial species: diversity and description through genomics. - Critical Reviews in Plant Sciences 39: 101-124. Go to original source...
  60. Whitton, B.A. (2012): Ecology of Cyanobacteria II: Their Diversity in Space and Time. - 760 pp., Springer, London. Go to original source...
  61. Wu, X.; Jiana, J.; Wan, Y.; Giesy, J.P. & Hua, J. (2012): Cyanobacteria blooms produce teratogenic retinoic acids. - Proceedings of the National Academy of Sciences of the United States of America 109: 9477-9482. Go to original source...
  62. Yamamoto, Y. (2011): Elucidating the adhesion and growth of the green alga Scenedsmus acutus under culture condition by using ultrasonic treatment. -Taiwania 56: 1-6.
  63. Yarza, P.; Yilmaz, P.; Pruesse, E.; Glöckner, F.O.; Ludwig, W.; Schleifer, K.; Whitman, W.B.; Euzéby, J.; Amann, R. & Rosselló-Móra, R. (2014): Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. - Nature Reviews Microbiology 12: 635-645. Go to original source...
  64. Żyszka-Haberecht, B.; Niemczyk, E. & Lipok, J. (2019): Metabolic relation of cyanobacteria to aromatic compounds. - Applied Microbiology and Biotechnology 103: 1167-1178. Go to original source...