Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2024-06-25
Page range: 125-143
Abstract views: 5
PDF downloaded: 0

A phylogenetically distant clade of Nostoc–like (Cyanobacteria) taxa with the description of Reofilinostoc matlalcueyense gen. et sp. nov. from an extreme environment

IZTA Herbarium
Unidad de Biotecnología y Prototipos (UBIPRO), Facultad de Estudios Superiores Iztacala, Universidad Nacional Autónoma de México (UNAM). Avenida de los Barrios No. 1, Col. Los Reyes Iztacala, Tlalnepantla, 54090, Estado de México, México.
Interdisciplinary Centre of Marine and Environmental Research, (CIIMAR/CIMAR-LA), Novo Edificio do Terminal de Cruzeiros do Porto de Leixões, Avenida General Norton de Matos, S/N, 4450-208, Matosinhos, Portugal.
IZTA Herbarium
Interdisciplinary Centre of Marine and Environmental Research, (CIIMAR/CIMAR-LA), Novo Edificio do Terminal de Cruzeiros do Porto de Leixões, Avenida General Norton de Matos, S/N, 4450-208, Matosinhos, Portugal. Department of Biology, Faculty of Sciences, Porto University, Rua do Campo Alegre, 4069-007 Porto, Portugal.
cryptic taxa elevation new genus Nodulariaceae Nostocaceae polyphasic approach stream cold Algae

Abstract

Although species of the order Nostocales have morphological similarities to each other, some Nostoc species have been considered cryptic and are classified in the families Nostocaceae, Nodulariaceae and Aphanizomenaceae. Since then, the phylogenetic and morphological evaluation of Nostoc-like organisms has led to the taxonomic revision of some genera in different families. In the present work a cyanobacterium morphologically identified as Nostoc was isolated from an extreme cold lotic environment, in a high mountain of the Transmexican Volcanic Belt, and was taxonomically and phylogenetically characterized based on a polyphasic approach. Analysis of the 16S rRNA gene sequence references: Reofilinostoc matlalcueyense gen. et sp. nov. Thus, establishing a new genus of the family Nodulariaceae. The morphology of Reofilinostoc in the wild is reminiscent of a mouse ear, it is of 0.4-1.2 cm in length and has a firm cartilaginous texture; colonies can be pale green, brown or dark green in colour. Through a microscopic inspection, the filaments resemble to Komarekiella atlantica, Desikacharya nostocoides and Minunostoc cylindricum. While, the phylogenetic approach yielded similar results and consistently showed that Reofilinostoc matlalcueyense F02 (OR724089) is closely related to D. nostocoides and M. cylindricum in the core clade of Nodulariaceae. This research revealed that some comparisons between genera of Nodulariaceae exhibited similarity values higher than 97%, such as Atlanticothrix vs. Goleter and Cyanocohniella vs. Anabaenopsis. Nevertheless, in comparison to these phylogenetically closer genera, a substantial difference in the length and structure of D1-D1’, Box-B and V3 helix was demostrated; where Reofilinostoc, Desikacharya, and Minunostoc are part of the Nodulariaceae family; leading to the establishment of Reofilinostoc gen. nov., with Reofilinostoc matlalcueyense sp. nov. as the type species.

References

  1. Alvarenga, D.O., Andreote, A.P.D., Branco, L.H.Z., Delbaje, E., Cruz, R.B., de Mello-Varani, A. & Fiore, M.F. (2021) Amazonocrinis nigriterrae gen. nov., sp. nov., Atlanticothrix silvestris gen. nov., sp. nov. and Dendronalium phyllosphericum gen. nov., sp. nov., nostocacean cyanobacteria from Brazilian environments. International Journal of Systematic and Evolutionary Microbiology 71 (5): 3329–3338. https://doi.org/10.1099/ijsem.0.004811
  2. Bagchi, S.N., Dubey, N. & Singh, P. (2017) Phylogenetically distant clade of Nostoc-like taxa with the description of Aliinostoc gen. nov. and Aliinostoc morphoplasticum sp. nov. International Journal of Systematic and Evolutionary Microbiology 67 (9): 3329–3338. https://doi.org/10.1099/ijsem.0.002112
  3. Barker, G.L.A., Hayes, P.K., O´Mahony, S.I., Vacharapiyasophon, P. & Walsby, A.E. (1999) A molecular and phenotypic analysis of Nodularia (Cyanobacteria) from the Baltic Sea. Journal Phycology 35: 931–937. https://doi.org/10.1046/j.1529-8817.1999.3550931.x
  4. Becerra-Absalón, I. & Tavera, R. (2009) Life cycle of Nostoc sphaericum (Nostocales, Cyanoprocaryota) in tropical wetlands. Nova Hedwigia 88: 117–128. https://doi.org/10.1127/0029-5035/2009/0088-0117
  5. Becerra-Absalón, I., Buhse, T., Polanco, C. & Tavera, R. (2012) Effect of Nitrogen and Periphyton Extract on the grow of Nostoc sphaericum in cultures. International Scholarly Research Network [ISRN] Ecology 2012: 935476. https://doi.org/10.5402/2012/935476
  6. Becerra-Absalón, I., Muñoz-Martin, M.Á. Montejano, G. & Mateo, P. (2019) Differences in the Cyanobacterial Community Composition of Biocrust From the Drylands of Central Mexico. Are There Endemic Species? Frontiers in Microbiology 10: 937. https://doi.org/10.3389/fmicb.2019.00937
  7. Bohunická, M., Pietrasiak, N., Johansen, J.R., Gómez, E.B., Hauer, T., Lira, A.G. & Lukešová, A. (2015) Roholtiella, gen. nov. (Nostocales, Cyanobacteria)—a tapering and branching cyanobacteria of the family Nostocaceae. Phytotaxa 197: 84–103. http://dx.doi.org/10.11646/phytotaxa.197.2.2
  8. Cai, F., Li, X., Geng, R., Peng, X. & Li, R. (2019a) Phylogenetically distant clade of Nostoc-like taxa with the description of Minunostoc gen. nov. and Minunostoc cylindricum sp. nov. Fottea Olomouc 19 (1): 13–24. http://doi.org/10.5507/fot.2018.013
  9. Cai, F., Li, X., Yang, Y., Jia, N., Huo, D. & Li, R. (2019b) Compactonostoc shennongjiaensis gen. et sp. nov. (Nostocales, Cyanobacteria) from a wet rocky wall in China. Phycologia 58: 200–210. https://doi.org/10.1080/00318884.2018.1541270
  10. Cai, F., Peng, X. & Li, R. (2020) Violetonostoc minutum gen. et sp. nov. (Nostocales, Cyanobacteria) from a rocky substrate in China. Algae 35 (1): 1–15. https://doi.org/10.4490/algae.2020.35.3.4
  11. Carmona-Jiménez, J. & Caro-Borrero, A. (2017) The last peri-urban rivers of the Mexico Basin: establishment of potential reference conditions through the evaluation of ecological quality and biological indicators. Revista Mexicana de Biodiversidad 88: 425–436. http://doi.org/10.1016/j.rmb.2017.03.019
  12. Carmona-Jiménez, J., Caro-Borrero, A., Becerra-Absalón, I., Perona-Urizar, E., Márquez Santamaría, K. & Mateo-Ortega, P. (2023) Description of two new species of Nostoc (Nostocales, Cyanobacteria) from central Mexico, using morphological, ecological, and molecular attributes. Journal of Phycology 59 (6): 1237–1257. https://doi.org/10.1111/jpy.13401
  13. Evans, R.D. & Johansen, J.R. (1999) Microbiotic Crust and Ecosystem Processes. Critical Reviews in Plant Sciences 18 (2): 183–225. https://doi.org/10.1080/07352689991309199
  14. Genuário, D.B., Marc, M.G.¸ Vaz al V., 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
  15. Guiry, M.D. & Guiry, G.M. (2023) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. Available from: http://www.algaebase.org (accessed: 26 March 2024).
  16. Hentschke, G.S., Johansen, J.R., Pietrasiak, N., Rigonato, J., Fiore, M.F. & Sant’Anna, C.L. (2017) Komarekiella atlantica gen et sp. nov. (Nostocaceae, Cyanobacteria): a new subaerial taxon from the Atlantic Rainforest and Kauai, Hawaii. Fottea Olomouc 17 (2): 178–190. http://dx.doi.org/10.5507/fot.2017.002
  17. 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 Olomouc 13 (2): 201–213. https://doi.org/10.5507/fot.2013.016
  18. Ibarra-Gallardo, C.E. & Novelo, E. (2018) Algas y cianoprocariontes epilíticos de la Zona Arqueológica de Yaxchilán, Chiapas, México. Revista Mexicana de Biodiversidad 89: 590–603. https://doi.org/10.22201/ib.20078706e.2018.3.2290
  19. Iteman, I., Rippka, R., Tandeau de Marsac, N. & Herdman, M. (2000) Comparison of conserved structural and regulatory domains within divergent 16S rRNA-23S rRNA spacer sequence of cyanobacteria. Microbiology 146 (5): 1275–1286. https://doi.org/10.1099/00221287-146-6-1275
  20. Kaštovský, J., Berrendero-Gomez, E., Hladil, J. & Johansen, J.R. (2014) Cyanocohniella calida gen et sp. nov. (Cyanobacteria: Aphanizomenonaceae a new cyanobacterium from the thermal springs from Karlovy Vary, Czech Republic. Phytotaxa 181 (5): 279–292. http://dx.doi.org/10.11646/phytotaxa.181.5.3
  21. Katoh, K., Kazuharu, M., Kuma, K. & Miyata, T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30 (14): 3059–3066. https://doi.org/10.1093/nar/gkf436
  22. Komárek, J. (2013) Cyanoprokaryota. 3rd. part: Heterocytous Genera. In: Büdel, B., Gärtner, G., Krienitz, L. & Schagerl, M. (Eds.) Süßwasserflora von Mitteleuropa 19/3. Springer, Spektrum Berlin, Heidelberg. 1130 pp.
  23. Komárek, J., Kaštovský, J., Mareš, J. & Johansen, J.R. (2014) Taxonomic classification of cyanoprokaryotes (Cyanobacterial genera) 2014 according to the polyphasic approach. Preslia 86: 295–335.
  24. Kumar, N., Saraf, A., Pal, S., Mishra, D. & Singh, P. (2022) Insights into the phylogenetic inconsistencies of the genus Amazonocrinis and description of epilithic Amazonocrinis malviyae sp. nov. (Cyanobacteria, Nostocales) from Jammu and Kashmir, India. International Journal of Systematic and Evolutionary Microbiology 72 (12). https://doi.org/10.1099/ijsem.0.005658
  25. Lee, N.J., Bang, S.D., Kim, T., Ki, J.S. & Lee, O.M. (2021) Pseudoaliinostoc sejongens gen. & sp. nov. (Nostocales, Cyanobacteria) from floodplain soil of the Geum River in Korea based on a polyphasic approach. Phytotaxa 472 (1): 55–70. https://doi.org/10.11646/phytotaxa.479.1.4
  26. Lepère, C., Wilmotte, A. & Meyer, B. (2000) Molecular diversity of Microcystis strains (Cyanophyceae, Chroococcales) based on 16S rDNA sequences. Systematic and Geography of Plants 70: 275–283. https://doi.org/10.2307/3668646
  27. López-Adrián, S.J. & Catzim, C.L.A. (2010) Microalgas dulceacuícolas. In: Duran García, R. & Méndez González, M.E. (Eds.) Biodiversidad y desarrollo humano en Yucatán. CICY, PPD-FMAM, CONABIO, SEDUMA, Mérida. pp. 185–186.
  28. Lukešová, A., Johansen, J.R., Martin, M.P. & Casamatta, D.A. (2009) Aulosira bohemensis sp. nov.: Further phylogenetic uncertainty at the base of the Nostocales (Cyanobacteria). Phycologia 48 (2): 118–129. https://doi.org/10.2216/08-56.1
  29. Luz, R., Hentschke, G.S., Cordeiro, R., Fonseca, A., Urbatzka, R., Vasconcelos, V. & Gonçalves, V. (2024) Description of Azorothrix ramosa gen. et sp. nov. (Tolypotrichaceae, Cyanobacteria), a new Tolypotrichaceae from Atlantic oceanic islands. Fottea 24 (1): 99–108. https://doi.org/10.5507/fot.2023.04
  30. Macek, M., Vilaclara-Fatjó, G., Lugo-Vázquez, A. & Alcocer-Durand, J. (2007) Lago de Atexcac. In: De la Lanza Espino, G. & Hernández Pulido, S. (eds.) Las aguas interiores de México: conceptos y casos. AGT Editor, México. pp. 199–212.
  31. Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE). pp. 1–8. https://doi.org/10.1109/GCE.2010.5676129
  32. Miscoe, L.H., Johansen, J.R., Vaccarino, M.A., Pietrasiak, N. & Sherwood, A.R. (2016) The diatom flora and cyanobacteria from caves on Kauai, Hawaii. II. Novel cyanobacteria from caves on Kauai. Hawaii. Biblotheca Phycologia 123: 75–152.
  33. Mishra, D., Saraf, A., Kumar, N., Pal, S. & Singh, P. (2021) Issues in cyanobacterial taxonomy: comprehensive case study of unbranched, false branched and true branched heterocystous cyanobacteria. FEMS Microbiology Letters 3 (368): fnab005. https://doi.org/10.1093/femsle/fnab005
  34. Montejano-Zurita, G. & González-González, J. (1981) Notas sobre la variación y ciclos de vida de Nostoc. Phycologia Latinoamericana 1: 47–59.
  35. Neilan, B.A., Jacobs, D., Del Dot, T., 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 Bacteriology 47 (3): 693–697. https://doi.org/10.1099/00207713-47-3-693
  36. Novelo, E. (2011) Flora del Valle de Tehuacán-Cuicatlán. Fascículo 90. Cyanoprokaryota. Universidad Nacional Autónoma de México. Instituto de Biología. México. 96 pp.
  37. Nübel, U., Garcia-Pichel, F. & Muyzer, G. (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Applied and Environmental Microbiology Journal. 63: 3327–3332. https://doi.org/10.1128%2Faem.63.8.3327-3332.1997
  38. Oliva-Martínez, M.G., Lugo-Vázquez, A., Alcocer-Durand, J., Peralta, L. & Oseguera, L.A. (2009) Planktonic Bloom-Forming Nodularia in the Saline Lake Alchichica, Mexico. Natural Resources and Environmental Issues 15: 121–126. Available from: https://digitalcommons.usu.edu/nrei (accessed 24 June 2024)
  39. Ortega, M.M. (1984) Catálogo de algas continentales recientes de México. Universidad Nacional Autónoma de México, México. 566 pp.
  40. Price, M.N., Dehal, P.S. & Arkin, A.P. (2009) FastTree: Computing Large Minimum-Evolution Trees with Profiles instead of a Distance Matrix. Molecular Biology and Evolution 26: 1641–1650. https://doi.org/10.1093/molbev/msp077
  41. Ramírez, M., Hernández-Mariné, M., Novelo, E. & Roldán, M. (2010) Cyanobacteria containing biofilms from a Mayan monument in Palenque Mexico. Biofouling 26 (4): 399–409. https://doi.org/10.1080/08927011003660404
  42. Ramírez, M., Hernández-Mariné, M., Mateo, P., Berrendero, E. & Roldán, M. (2011) Polyphasic approach and adaptive strategies of Nostoc cf. commune (Nostocales, Nostocaceae) growing on Maya monuments. Fottea 11 (1): 73–86. https://doi.org/10.5507/fot.2011.008
  43. Rajaniemi, P., Hrouzek, P., Kaštovská, 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. https://doi.org/10.1099/ijs.0.63276-0
  44. Řeháková, K., Johansen, J.R., Casamatta, D.A., Xuesong, L. & Vincent, J. (2007) Morphological and molecular characterization of selected desert soil cyanobacteria: three species new to science including Mojavia pulchra gen. et sp. nov. Phycologia 46 (5): 481–502. https://doi.org/10.2216/06-92.1
  45. Řeháková, K., Johansen, J.R., Bown, M.B., Martin, M.P. & Sheil, C.A. (2014a) Variation in secondary structure of the 16S rRNA molecule in cyanobacteria with implications for phylogenetic analysis. Fottea 14 (2): 161–178. https://doi.org/10.5507/fot.2014.013
  46. Řeháková, K., Mareš, J., Lukešová, A., Zapomělová, E., Bernardova, K. & Hrouzek, P. (2014b) Nodularia (Cyanobacteria, Nostocaceae): a phylogenetically uniform genus with variable phenotypes. Phytotaxa172 (3): 235–246. http://dx.doi.org/10.11646/phytotaxa.172.3.4
  47. 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
  48. Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. & Huelsenbeck, J.P. (2012) MrBayes 15 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61 (3): 539–542. https://doi.org/10.1093/sysbio/sys029
  49. Rodríguez-Flores, R. & Carmona-Jiménez, J. (2018) Ecology and distribution of macroscopic algae communities in streams from the Basin of Mexico. Botanical Sciences 96 (1): 63–75. https://doi.org/10.17129/botsci.1237
  50. Saraf, A., Dawda, H.G. & Singh, P. (2019a) Desikacharya gen. nov., a phylogenetically distinct genus of Cyanobacteria along with the description of two new species, Desikacharya nostocoide sp. nov., and Desikacharya soli sp. nov., and reclassification of Nostoc thermotolerans to Desikacharya thermotolerans comb. nov. International Journal of Systematic and Evolutionary Microbiology 69 (2): 307–315. https://doi.org/10.1099/ijsem.0.003093
  51. Saraf, A., Dawda, H.G. & Singh, P. (2019b) Validation of the genus Desikacharya gen. nov. (Nostocaceae, Cyanobacteria) and three included species. Notulae Algarum 107: 1–3, figs 1–8.
  52. Silveira, S.B., Wasielesky, W., Andreote, A.P.D., Fiore, M.F. & Odebrecht, C. (2017) Morphology, phylogeny, growth rate and nodularin production of Nodularia spumigena from Brazil, Marine Biology Research 13 (10): 1095–1107. https://doi.org/10.1080/17451000.2017.1336587
  53. Singh, P., Shaikh, Z.M., Gaysina, L.A., Surakar, A. & Smanta, U. (2016) New species of Nostoc (cyanobacteria) isolated from Pune, India, using morphological, ecological and molecular attributes. Plant Systematics and Evolution 302: 1381–1394. [https://www.jstor.org/stable/44853366]
  54. Shishido, T.K., Popin, R.V., Jokela, J., Walsten, M., Fiore, M.F., Fewer, D.P., Herfindal, L. & Sivonen, K. (2020) Dereplication of natural products with antimicrobial and anticancer activity from Brazilian cyanobacteria. Toxins 12 (1): 12. https://doi.org/10.3390/toxins12010012
  55. Soares, F., Ramos, V., Trovão, J., Cardosa, S.M., Tiago, I. & Portugal, A. (2021) Parakomarekiella sesnandensis gen. et sp. nov. (Nostocales, Cyanobacteria) isolated from the Old Cathedral of Coimbra, Portugal (UNESCO World Heritage Site). European Journal of Phycology 56 (3): 301–315. https://doi.org/10.1080/09670262.2020.1817568
  56. Stackebrandt, E. & Ebers, J. (2006) Taxonomic parameters revisited: Tarnished gold standards. Microbiology Today 33: 152–155.
  57. Strunecký, O., Ivanova, A.P. & Mareš, J. (2023) An updated classification of cyanobacterial orders and families based on phylogenomic and polyphasic analysis. Journal of Phycology 59 (1): 12–51. https://doi.org/10.1111/jpy.13304
  58. Tamura, K., Stecher, G. & Kumar, S. (2021) MEGA11: Molecular Evolutionary Genetics Analysis version 11. Molecular Biology and Evolution 38: 3022–3027. https://doi.org/10.1093/molbev/msab120
  59. Trifinopoulos, J., Nguyen, L.T., Von Haeseler, A. & Minh, B.Q. (2016) W- 421 IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research 44 (W1): 232–235. https://doi.org/10.1093/nar/gkw256
  60. Thiers, B. (2020) Index Herbariorum. A Global Directory of Public Herbaria and Associated Staff. New York Botanical Garden’s Virtual Herbarium. Available at: http://sweetgum.nybg.org/science/ih (accessed 24 June 2024)
  61. Xiao, Y., Zhang, X. & Ji, P. (2015) Modeling Forest Fire Occurrences Using Count-Data Mixed Models in Qiannan Autonomous Prefecture of Guizhou Province in China. PLoS ONE 10 (3): e0120621. https://doi.org/10.1371/journal.pone.0120621
  62. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research 31 (13): 3406–3415. https://doi.org/10.1093/nar/gkg595