1887

Abstract

In Iran, polyphasic studies of unicellular cyanobacteria are still scarce, with more emphasis being placed on filamentous cyanobacteria in paddy fields and fresh water regions. In an effort to increase the knowledge of the diversity of unicellular cyanobacteria from paddy fields in Iran, we have isolated and characterized a new unicellular cyanobacterium strain. The strain was studied using a polyphasic approach based on morphological, ecological and phylogenetic analyses of the 16S–23S ITS rRNA gene region. Complementarily, we have searched for the presence of cyanotoxin genes and analysed the pigment content of the strain. Results showed that the strain was morphologically indistinguishable from the genus , but phylogenetic analyses based on the Bayesian inference and maximum-likelihood methods placed the strain in a separated monophyletic and highly supported (0.99/98, posterior probability/maximum-likelihood) genus-level cluster, distant from and with as sister taxa. The calculated -distance for the 16S rRNA gene also reinforced the presence of a new genus, by showing 92 % similarity to . The D1–D1′, Box-B and V3 ITS secondary structures showed the uniqueness of this strain, as it shared no similar pattern with closest genera within the Chroococcales. For all these reasons, and in accordance with the International Code of Nomenclature for Algae, Fungi and Plants, we here proposed the description of a new genus with the name gen. nov. along with the description of a new species, sp. nov. (holotype: CCC1399-a; reference strains CCC1399-b; MCC 4116).

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004828
2021-06-07
2024-12-03
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/71/6/ijsem004828.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.004828&mimeType=html&fmt=ahah

References

  1. Price GD, Badger MR, Woodger FJ, Long BM. Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. J Exp Bot 2007; 59:1441–1461 [View Article][PubMed]
    [Google Scholar]
  2. Nowruzi B, Haghighat S, Fahimi H, Mohammadi E. Nostoc cyanobacteria species: a new and rich source of novel bioactive compounds with pharmaceutical potential. J Pharm Health Serv Res 2018; 9:5–12 [View Article]
    [Google Scholar]
  3. Liu L, Jokela J, Wahlsten M, Nowruzi B, Permi P. Nostosins, trypsin inhibitors isolated from the terrestrial Cyanobacterium nostoc sp. strain FSN. J Nat Prod 2014; 77:1784–1790 [View Article][PubMed]
    [Google Scholar]
  4. Komárek J, Anagnostidis K. Cyanoprokaryota 1. Teil: Chroococcales. Ettl H, Gärtner G, Heynig H. eds In Süsswasserflora von Mitteleuropa 19/1 Germany: Gustav Fischer, Jena-StuttgartLübeck-Ulm; 1998 pp 1–548
    [Google Scholar]
  5. Cyanoprokaryota KJ. 3. Heterocytous genera. Büdel B, Gärtner G, Krienitz L, Schagerl M. eds In Süswasserflora von Mitteleuropa/Freshwater flora of Central Europe Berlin/Heidelberg/Germany: Springer Spektrum; pp 1–1130
    [Google Scholar]
  6. Dvořák P, Casamatta DA, Hašler P, Jahodářová E, Norwich AR et al. Diversity of the cyanobacteria. Hallenbeck P. eds In Modern Topics in the Phototrophic Prokaryotes Springer International Publishing; 2017 p 350
    [Google Scholar]
  7. Wilmotte A, Herdman M. Phylogenetic relationships among the cyanobacteria based on 16s rRNA sequences. In Bergey’s Manual of systematic Bacteriology. Volume one: The Archaea and the Deeply Branching and Phototrophic Bacteria pp 487–493
    [Google Scholar]
  8. Casamatta DA, Vis ML. Flow rate and nutrient level effects on the morphology of Phormidium retzii (Cyanobacteria) in artificial stream mesocosms. Algol Stud 2004; 113:87–99
    [Google Scholar]
  9. Perkerson RB, Johansen JR, Kováčik L, Brand J, Kaštovskỳ J et al. A unique pseudanabaenalean (cyanobacteria) genus Nodosilinea gen. nov. based on morphological and molecular data. J Phycol 2011; 47:1397–1412
    [Google Scholar]
  10. Haande S, Rohrlack T, Ballot A, Røberg K, Skulberg R. Genetic characterisation of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) isolates from Africa and Europe. Harmful Algae 2008; 7:692–701 [View Article]
    [Google Scholar]
  11. Mollenhauer D, Büdel B, Mollenhauer R. Approaches to species delimitations in the genus Nostoc Vaucher 1803 ex Bornet et Flahault 1888. Algol Stud 1994; 75:189–209
    [Google Scholar]
  12. Korelusová J. Phylogeny of heterocystous Cyanobacteria (Nostocales and Stigonematales). PhD thesis University of South Bohemia, České Budějovice; 2008
    [Google Scholar]
  13. Aboal M, Werner O, García-Fernández ME, Palazón JA, Cristóbal C et al. Should ecomorphs be conserved? The case of Nostoc flagelliforme, an endangered extremophile cyanobacteria. J Nat Conserv 2016; 30:52–64 [View Article]
    [Google Scholar]
  14. Komárek J, Kaštovskỳ J, Mareš J, Johansen JR. Taxonomic classification of cyanoprokaryotes (cyanobacterial genera), using a polyphasic approach. Preslia 2014; 86:295–335
    [Google Scholar]
  15. Zapomělová E, Skácelová O, Pumann P, Kopp R, Janeček E. Biogeographically interesting planktonic Nostocales (Cyanobacteria) in the Czech Republic and their polyphasic evaluation resulting in taxonomic revisions of Anabaena bergii Ostenfeld 1908 (Chrysosporum gen. nov.) and A. tenericaulis Nygaard 1949 (Dolichospermum tenericaule comb. nova. Hydrobiologia 2012; 698:353 [View Article]
    [Google Scholar]
  16. Vandamme P, Pot B, Gillis M, de Vos P, Kersters K et al. Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol Rev 1996; 60:407–438 [View Article][PubMed]
    [Google Scholar]
  17. Johansen JR, Casamatta DA. Recognizing cyanobacterial diversity through adoption of a new species paradigm. Algol Stud 2005; 117:71–93
    [Google Scholar]
  18. Komárek J. A polyphasic approach for the taxonomy of cyanobacteria: principles and applications. Eur J Phycol 2016; 51:346–353 [View Article]
    [Google Scholar]
  19. Hauer T, Bohunická M, Johansen JR, Mareš J, Berrendero-Gomez E. Reassessment of the cyanobacterial family Microchaetaceae and establishment of the new families Tolypothrichaceae and Godleyaceae . J Phycol 2014; 50:1089–1100 [View Article][PubMed]
    [Google Scholar]
  20. Dvořák P, Jahodářová E, Hašler P, Gusev E, Poulíčková A. A new tropical cyanobacterium Pinocchia polymorpha gen. et sp. nov. derived from genus Pseudanabaena . Fottea 2015; 15:113–120
    [Google Scholar]
  21. Hašler P, Casamatta D, Dvořák P, Poulíčková A. Jacksonvillea apiculata (Oscillatoriales, Cyanobacteria) gen. & sp. nov.: a new genus of filamentous, epipsamic cyanobacteria from North Florida. Phycologia 2017; 56:284–295
    [Google Scholar]
  22. Nowruzi B, Khavari-Nejad RA, Sivonen K, Kazemi B, Najafi F. Identification and toxigenic potential of a Nostoc sp. Algae 2012; 27:303–313 [View Article]
    [Google Scholar]
  23. Nowruzi B, Khavari-Nejad RA, Sivonen K, Kazemi B, Najafi F. Identification and toxigenic potential of a cyanobacterial strain (Anabaena sp. Prog Biol Sci 2013; 3:79–85
    [Google Scholar]
  24. Nowruzi B, Fahimi H, Ordodari N. Molecular phylogenetic and morphometric evaluation of Calothrix sp. N42 and Scytonema sp. N11. Rostaniha 2017; 18:210–221
    [Google Scholar]
  25. Nowruzi B, Blanco S, Nejadsattari T. Chemical and molecular evidences for the poisoning of a duck by Anatoxin-a, Nodularin and Cryptophycin at the coast of the ShoorMast Lake (Mazandaran province, Iran). Int J Algae 2018; 20:359–376
    [Google Scholar]
  26. Nowruzi B, Blanco S. In silico identification and evolutionary analysis of candidate genes involved in the biosynthesis methylproline genes in cyanobacteria strains of Iran. Phytochem Lett 2019; 29:199–211
    [Google Scholar]
  27. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier R. Generic assignments, strain histories and properties of pure cultures of Cyanobacteria . . Microbiology 1979; 111:1–61 [View Article]
    [Google Scholar]
  28. Neilan BA, Jacobs D, Del Dot T, Blackall LL, Hawkins PR. Relationships among toxic and nontoxic cyanobacteria of the genus Microcystis . Int J Syst Bacteriol 2007; 47:693–697
    [Google Scholar]
  29. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1995; 215:403–410
    [Google Scholar]
  30. Roldán M, Ramírez M, del Campo J, Hernández-Mariné M, Komárek J. Chalicogloea cavernicola gen. nov. sp. nov. (Chroococcales, Cyanobacteria) from low light aerophytic environments: Combined molecular, phenotypic and ecological criteria. Int J Syst Evol Micr 2012; 63:2326–2333
    [Google Scholar]
  31. Katoh K, Rozewicki J, Yamada KD. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 2019; 20:1160–1166 [View Article][PubMed]
    [Google Scholar]
  32. Okonechnikov K, Golosova O, Fursov M. Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics 2012; 28:1166–1167 [View Article][PubMed]
    [Google Scholar]
  33. Nylander JAA. Mrmodeltest v2.3 Program Distributed by the Author Evolutionary Biology Centre. Uppsala University; 2004
    [Google Scholar]
  34. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 2012; 61:539–542 [View Article][PubMed]
    [Google Scholar]
  35. Rambaut A, Drummond AJ. FigTree: Tree figure drawing tool, v. 1.2.2; 2008 http://tree.bio. ed.ac.uk/software/figtree/
  36. Trifinopoulos J, Nguyen LT, Haeseler von, Minh BQ. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res 2016; 44:W232–W235 [View Article]
    [Google Scholar]
  37. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003; 31:3406–3415 [View Article][PubMed]
    [Google Scholar]
  38. Lowe TM, Chan PP. tRNAscan-SE on-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Res 2016; 44:W54–W57
    [Google Scholar]
  39. Rantala A, Fewer DP, Hisbergues M, Rouhiainen L, Vaitomaa J et al. Phylogenetic evidence for the early evolution of microcystin synthesis. Proc Natl Am Soc 2004; 101:568–573 [View Article]
    [Google Scholar]
  40. Fewer DP, Rouhiainen L, Jokela J, Wahlsten M, Laakso K et al. Recurrent adenylation domain replacement in the microcystin synthetase gene cluster. BMC Evol Biol 2007; 7:183 [View Article][PubMed]
    [Google Scholar]
  41. Nowruzi B, Fahimi H, Lorenzi AS. Recovery of pure C-phycoerythrin from a limestone drought tolerant cyanobacterium Nostoc sp. and evaluation of its biological activity. Anales de Biología 2020; 42:115–128
    [Google Scholar]
  42. Afreen S, Fatma T. Extraction, purification and characterization of phycoerythrin from Michrochaete and its biological activities. Biocatal Agric Biotechnol 2018; 13:84–89
    [Google Scholar]
  43. Chakdar H, Pabbi S. Extraction and purificationof phycoerythrin from Anabaena variabilis (CCC 421 Phykos 2012; 42:25–31
    [Google Scholar]
  44. Tiwari ON, Devi WI, Silvia C, Devi AT, Gunapati Oinam OAS et al. Modulation of phycobiliprotein production in Nostoc muscorum through culture manipulation.” Journal of Applied Biology and Biotechnology 3 2015 pp 011–016
  45. Román RB, Alvarez-Pez JM, Fernández FA, Grima EM. Recovery of pure B-phycoerythrin from the microalga Porphyridium cruentum. J Biotechnol 2002; 93:73–85
    [Google Scholar]
  46. Garcia-Pichel F, Nubel U, Muyzer G. The phylogeny of unicellular, extremely halotolerant cyanobacteria. Arch Microbiol 1998; 169:469–482 [View Article][PubMed]
    [Google Scholar]
  47. Komárek J. Recent changes (2008) in cyanobacteria taxonomy based on a combination of molecular background with phenotype and ecological consequences (genus and species concept). Hydrobiologia 2010; 639:245–259
    [Google Scholar]
  48. Boyer SL, Flechtner VR, Johansen JR. 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 2001; 18:1057–1069 [View Article][PubMed]
    [Google Scholar]
  49. Casamatta DA, Gomez SR, Johansen JR. Rexia erecta gen. et sp. nov. and Capsosira lowei sp. nov., two newly described cyanobacterial taxa from the Great Smoky Mountains National Park (USA. Hydrobiologia 2006; 561:13–26 [View Article]
    [Google Scholar]
  50. Johansen JR, Kovacik L, Casamatta DA, Fučiková K, Kaštovský J. 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 2001; 92:283–302
    [Google Scholar]
  51. Komarkova J, Zapomelova E, Komarek J. Chakia (cyanobacteria), a new heterocytous genus from belizean marshes identified on the basis of the 16S rrna gene. Fottea 2013; 13:227–233 [View Article]
    [Google Scholar]
  52. Hašler P, Dvořák P, Poulíčková A, Casamatta DA. A novel genus Ammassolinea gen. nov. (Cyanobacteria) isolated from sub-tropical epipelic habitats. Fottea 2014; 14:241–248 [View Article]
    [Google Scholar]
  53. Aguilera A, Gómez EB, Kaštovský J, Echenique RO, Salerno GL. The polyphasic analysis of two native Raphidiopsis isolates supports the unification of the genera Raphidiopsis and Cylindrospermopsis (Nostocales, Cyanobacteria). Phycologia 2018; 57:130–146
    [Google Scholar]
  54. Komárková J, Jezberová J, Komárek O, Zapomělová E. Variability of Chroococcus (Cyanobacteria) morphospecies with regard to phylogenetic relationships. Hydrobiologia 2010; 639:69–83 [View Article]
    [Google Scholar]
  55. Kováčik L, Jezberová J, Komárková J, Kopecký J, Komárek J. Ecological characteristics and polyphasic taxonomic classification of stable pigment-types of the genus Chroococcus (Cyanobacteria . Preslia 2011; 83:145–166
    [Google Scholar]
  56. Gama WA, Rigonato J, Fiore MF, Sant’Anna CL. New insights into Chroococcus (Cyanobacteria) and two related genera: Cryptococcum gen. nov and Inacoccus gen. nov .. Eur J Phycol 2019; 54:315–325
    [Google Scholar]
  57. Börner T, Dittmann E. Molecular biology of cyanobacterial toxins. Huisman J, Matthijs H, Visser P. eds In Harmful Cyanobacteria Berlin: Springer; 2005 pp 25–40
    [Google Scholar]
  58. Jungblut AD, Neilan BA. Molecular identification and evolution of the cyclic peptide hepatotoxins, microcystin and nodularin, synthetase genes in three orders of cyanobacteria. Arch Microbiol 2006; 185:107–114 [View Article][PubMed]
    [Google Scholar]
  59. Sipari H, Rantala-Ylinen A, Jokela J, Oksanen I, Sivonen K. Development of a chip assay and quantitative PCR for detecting microcystin synthetase E gene expression. Appl Environ Microbiol 2010; 76:3797–3805 [View Article][PubMed]
    [Google Scholar]
  60. Sivonen K, Börner T. Bioactive compounds produced by cyanobacteria. Herrero A A, Flores E. eds In The Cyanobacteria: Molecular Biology, Genomics and Evolution Norfolk: Caister Academic Press; 2008 pp 159–197
    [Google Scholar]
  61. Weller DI. Detection, identification and toxigenicity of cyanobacteria in New Zealand lakes using PCR-based methods. N Z J Mar Freshwater Res 2011; 45:651–664
    [Google Scholar]
  62. Cuzman OA, Ventura S, Sili C, Mascalchi C, Turchetii T. Biodiversity of phototrophic biofilms dwelling on monumental fountains. Microb Ecol 2010; 60:81–95 [View Article][PubMed]
    [Google Scholar]
/content/journal/ijsem/10.1099/ijsem.0.004828
Loading
/content/journal/ijsem/10.1099/ijsem.0.004828
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error