1887

Abstract

This work characterizes a unicellular cyanobacterium with nearly spherical cells and thin-outlined sheaths that divide irregularly, forming small packets immersed in a diffluent mucilaginous layer. It was isolated growing on calcite speleothems and walls in a show cave in Collbató (Barcelona, Spain). Spectral confocal laser and transmission electron microscopy were used to describe the morphology, fine structure and thylakoid arrangement. The pigments identified were phycoerythrin, phycocyanin, allophycocyanin and chlorophyll . Three-dimensional reconstructions, generated from natural fluorescence -stacks, revealed a large surface area of nearly flat, arm-like thylakoidal membranes connected to each other and forming a unified structure in a way that, to our knowledge, has never been described before. Phylogenetic analyses using the 16S rRNA gene sequence showed 95 % similarity to strain sp. JJCM (GenBank accession no. AM710384). The diacritical phenotypic features do not correspond to any species currently described, and the genetic traits support the strain being classified as the first member of an independent genus in the order Chroococcales and the family Chroococcaceae. Hence, we propose the name gen. nov., sp. nov. under the provisions of the International Code of Nomenclature for Algae, Fungi and Plants. The type strain of is COLL 3 ( = CCALA 975  = CCAP 1424/1).

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2013-06-01
2024-04-18
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References

  1. Abed R. M. M., Garcia-Pichel F., Hernández-Mariné M. ( 2002 ). Polyphasic characterization of benthic, moderately halophilic, moderately thermophilic cyanobacteria with very thin trichomes and the proposal of Halomicronema excentricum gen. nov., sp. nov.. Arch Microbiol 177, 361370. [View Article] [PubMed]
    [Google Scholar]
  2. Albertano P., Hernández-Mariné M. ( 2001 ). Algae in habitats with reduced and extreme radiation. . Nova Hedwigia 123, 225227.
    [Google Scholar]
  3. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. ( 1997 ). Gapped blast and psi-blast: a new generation of protein database search programs. . Nucleic Acids Res 25, 33893402. [View Article] [PubMed]
    [Google Scholar]
  4. Anagnostidis K., Pantazidou A. ( 1991 ). Marine and aerophytic Cyanosarcina, Stanieria and Pseudocapsa (Chroococcales) species from Hellas (Greece). . Algol Stud 64, 141157.
    [Google Scholar]
  5. Berrendero E., Perona E., Mateo P. ( 2008 ). Genetic and morphological characterization of Rivularia and Calothrix (Nostocales, Cyanobacteria) from running water. . Int J Syst Evol Microbiol 58, 447460. [View Article] [PubMed]
    [Google Scholar]
  6. Brown I. I., Mummey D., Cooksey K. E. ( 2005 ). A novel cyanobacterium exhibiting an elevated tolerance for iron. . FEMS Microbiol Ecol 52, 307314. [View Article] [PubMed]
    [Google Scholar]
  7. Bryant D. ( 1982 ). Phycoerythrocyanin and phycoerythrin: properties and occurrence in cyanobacteria. . J Gen Microbiol 128, 835844.
    [Google Scholar]
  8. Castresana J. ( 2000 ). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. . Mol Biol Evol 17, 540552. [View Article] [PubMed]
    [Google Scholar]
  9. Cox G. C., Benson D., Dwarte D. M. ( 1981 ). Ultrastructure of cave-wall cyanophyte – Gloeocapsa NS4. . Arch Microbiol 130, 165174. [View Article]
    [Google Scholar]
  10. Decho A. W., Norman R. S., Visscher P. T. ( 2010 ). Quorum sensing in natural environments: emerging views from microbial mats. . Trends Microbiol 18, 7380. [View Article] [PubMed]
    [Google Scholar]
  11. Doyle J. J., Doyle J. L. ( 1987 ). A rapid DNA isolation for small quantities of fresh leaf tissue. . Phytochem Bull 19, 1115.
    [Google Scholar]
  12. Ferrera I., Massana R., Casamayor E. O., Balagué V., Sánchez O., Pedrós-Alió C., Mas J. ( 2004 ). High-diversity biofilm for the oxidation of sulfide-containing effluents. . Appl Microbiol Biotechnol 64, 726734. [View Article] [PubMed]
    [Google Scholar]
  13. Galtier N., Gouy M., Gautier C. ( 1996 ). seaview and phylo_win: two graphic tools for sequence alignment and molecular phylogeny. . Comput Appl Biosci 12, 543548.[PubMed]
    [Google Scholar]
  14. Garcia-Pichel F., Nübel U., Muyzer G. ( 1998 ). The phylogeny of unicellular, extremely halotolerant cyanobacteria. . Arch Microbiol 169, 469482. [View Article] [PubMed]
    [Google Scholar]
  15. Golubič S. ( 1967 ). Zwei wichtige Merkmale zur Abgrenzung der Blaualgengattungen. . Schweiz Ztschr Hydrol 29, 176184 (in German).
    [Google Scholar]
  16. Hernández-Mariné M., Roldán M., Clavero E., Canals A., Ariño X. ( 2001 ). Phototrophic biofilm morphology in dim light. The case of the Puigmolto sinkhole. . Nova Hedwigia 123, 237251.
    [Google Scholar]
  17. Hoffmann L., Komárek J., Kaštovský J. ( 2005 ). System of cyanoprokaryotes (cyanobacteria) – state in 2004. . Algol Stud 117, 95115. [View Article]
    [Google Scholar]
  18. Huelsenbeck J. P., Ronquist F. ( 2001 ). mrbayes: Bayesian inference of phylogenetic trees. . Bioinformatics 17, 754755. [View Article] [PubMed]
    [Google Scholar]
  19. Johansen J. R., Casamatta D. A. ( 2005 ). Recognizing cyanobacterial diversity through adoption of a new species paradigm. . Algol Stud 117, 7193. [View Article]
    [Google Scholar]
  20. Katoh K., Misawa K., Kuma K., Miyata T. ( 2002 ). mafft: a novel method for rapid multiple sequence alignment based on fast Fourier transform. . Nucleic Acids Res 30, 30593066. [View Article] [PubMed]
    [Google Scholar]
  21. Komárek J. ( 2010a ). Modern taxonomic revision of planktic nostocacean cyanobacteria: a short review of genera. . Hydrobiologia 639, 231243. [View Article]
    [Google Scholar]
  22. Komárek J. ( 2010b ). Recent changes (2008) in cyanobacteria taxonomy based on a combination of molecular background with phenotype and ecological consequences (genus and species concept). . Hydrobiologia 639, 245259. [View Article]
    [Google Scholar]
  23. Komárek J., Anagnostidis K. ( 1998 ). Cyanoprokaryota. Teil/Part 1: Chroococcales (Süßwasserflora von Mitteleuropa 19/1). Jena:: Gustav Fischer;.
    [Google Scholar]
  24. Komárek J., Kaštovský J. ( 2003 ). Coincidences of structural and molecular characters in evolutionary lines in cyanobacteria. . Algol Stud 109, 305325. [View Article]
    [Google Scholar]
  25. Komárek J., Cepák V., Kaštovský J., Sulek J. ( 2004 ). What are the cyanobacterial genera Cyanothece and Cyanobacterium? Contribution to the combined molecular and phenotype taxonomic evaluation of cyanobacterial diversity. . Algol Stud 113, 136. [View Article]
    [Google Scholar]
  26. Komárková J., Jezberová J., Komárek O., Zapomelová E. ( 2010 ). Variability of Chroococcus (Cyanobacteria) morphospecies with regard to phylogenetic relationships. . Hydrobiologia 639, 6983. [View Article]
    [Google Scholar]
  27. Kováčik L. ( 1988 ). Cell division in simple coccal cyanophytes. . Algol Stud 50–53, 149190.
    [Google Scholar]
  28. Lamprinou V., Pantazidou A., Papadogiannaki G., Radea C., Economou-Amili A. ( 2009 ). Cyanobacteria and associated invertebrates in Leontari cave. . Fottea 9, 155164. [CrossRef]
    [Google Scholar]
  29. Lang N. J., Whitton B. A. ( 1973 ). Arrangement and structure of thylakoids. . In The Biology of Blue-Green Algae, pp. 6679. Berkeley & Los Angeles:: University of California Press;.
    [Google Scholar]
  30. Lefèvre M., Laporte G., Bauer J. ( 1964 ). Sur les microorganismes envahissant les peintures rupestres de la grotte préhistorique de Lascaux. . C R Acad Sci 258, 51165118 (in French).
    [Google Scholar]
  31. Liberton M., Austin J. R. II, Berg R. H., Pakrasi H. B. ( 2011 ). Unique thylakoid membrane architecture of a unicellular N2-fixing cyanobacterium revealed by electron tomography. . Plant Physiol 155, 16561666. [View Article] [PubMed]
    [Google Scholar]
  32. Maidak B. L., Cole J. R., Lilburn T. G., Parker C. T. Jr, Saxman P. R., Farris R. J., Garrity G. M., Olsen G. J., Schmidt T. M., Tiedje J. M. ( 2001 ). The RDP-II (Ribosomal Database Project). . Nucleic Acids Res 29, 173174. [View Article] [PubMed]
    [Google Scholar]
  33. Mullineaux C. W. ( 1999 ). The thylakoid membranes of cyanobacteria: structure, dynamics and function. . Aust J Plant Physiol 26, 671677. [View Article]
    [Google Scholar]
  34. Nevo R., Charuvi D., Shimoni E., Schwarz R., Kaplan A., Ohad I., Reich Z. ( 2007 ). Thylakoid membrane perforations and connectivity enable intracellular traffic in cyanobacteria. . EMBO J 26, 14671473. [View Article] [PubMed]
    [Google Scholar]
  35. Nübel U., Garcia-Pichel F., Muyzer G. ( 2000 ). The halotolerance and phylogeny of cyanobacteria with tightly coiled trichomes (Spirulina Turpin) and the description of Halospirulina tapeticola gen. nov., sp. nov.. Int J Syst Evol Microbiol 50, 12651277. [View Article] [PubMed]
    [Google Scholar]
  36. Oren A. ( 2011 ). Cyanobacterial systematics and nomenclature as featured in the International Bulletin of Bacteriological Nomenclature and Taxonomy/International Journal of Systematic Bacteriology/International Journal of Systematic and Evolutionary Microbiology . . Int J Syst Evol Microbiol 61, 1015. [View Article] [PubMed]
    [Google Scholar]
  37. Ramírez M., Hernández–Mariné M., Mateo P., Berrenderro E., Roldán M. ( 2011 ). Polyphasic approach and adaptative strategies of Nostoc cf. commune (Nostocales, Nostocaceae) growing on Mayan monuments. . Fottea 11, 7386. [CrossRef]
    [Google Scholar]
  38. Ramos V., Seabra R., Brito A., Santos A., Santos C., Lopo M., Moradas-Ferreira P., Vasconcelos V. M., Tamagnini P. ( 2010 ). Characterization of an intertidal cyanobacterium that constitutes a separate clade together with thermophilic strains. . Eur J Phycol 45, 394403. [View Article]
    [Google Scholar]
  39. Roldán M., Hernández-Mariné M. ( 2009 ). Exploring the secrets of the three-dimensional architecture of phototrophic biofilms in caves. . Int J Speleol 38, 4153. [View Article]
    [Google Scholar]
  40. Roldán M., Clavero E., Castel S., Hernández-Mariné M. ( 2004a ). Biofilms fluorescence and image analysis in hypogean monuments research. . Algol Stud 111, 127143. [View Article]
    [Google Scholar]
  41. Roldán M., Thomas F., Castel S., Quesada A., Hernández-Mariné M. ( 2004b ). Noninvasive pigment identification in single cells from living phototrophic biofilms by confocal imaging spectrofluorometry. . Appl Environ Microbiol 70, 37453750. [View Article] [PubMed]
    [Google Scholar]
  42. Roldán M., Oliva F., Gónzalez del Valle M. A., Saiz-Jimenez C., Hernández-Mariné M. ( 2006 ). Does green light influence the fluorescence properties and structure of phototrophic biofilms?. Appl Environ Microbiol 72, 30263031. [View Article] [PubMed]
    [Google Scholar]
  43. Silva e Silva L. H., Damazio C. M., Iespa A. A. C. ( 2005 ). Composição cianobacteriana em trombólitos da lagoa Pitanguinha (Holoceno), Estado do Rio de Janeiro, Brasil. . Gaea 1, 7581 (in Portuguese).
    [Google Scholar]
  44. Stackebrandt E., Goebel B. M. ( 1994 ). Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. . Int J Syst Bacteriol 44, 846849. [View Article]
    [Google Scholar]
  45. Stamatakis A. ( 2006 ). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. . Bioinformatics 22, 26882690. [View Article] [PubMed]
    [Google Scholar]
  46. Stanier R. Y., Kunisawa R., Mandel M., Cohen-Bazire G. ( 1971 ). Purification and properties of unicellular blue-green algae (order Chroococcales). . Bacteriol Rev 35, 171205.[PubMed]
    [Google Scholar]
  47. Urzì C., De Leo F., Bruno L., Albertano P. ( 2010 ). Microbial diversity in paleolithic caves: a study case on the phototrophic biofilms of the Cave of Bats (Zuheros, Spain). . Microb Ecol 60, 116129. [View Article] [PubMed]
    [Google Scholar]
  48. Wilmotte A. ( 1994 ). Molecular evolution and taxonomy of the cyanobacteria. . In The Molecular Biology of Cyanobacteria, pp. 125. Edited by Bryant D. A. . Dordrecht:: Kluwer;. [View Article]
    [Google Scholar]
  49. Wilmotte A., Turner S., Van de Peer Y., Pace N. R. ( 1992 ). Taxonomic study of marine oscillatoriacean strains (cyanobacteria) with narrow trichomes. II: Nucleotide sequence analysis of the 16S ribosomal RNA. . J Phycol 28, 828838. [View Article]
    [Google Scholar]
  50. Wolf E., Schüßler A. ( 2005 ). Phycobiliprotein fluorescence of Nostoc punctiforme changes during the life cycle and chromatic adaptation: characterization by spectral confocal laser scanning microscopy and spectral unmixing. . Plant Cell Environ 28, 480491. [View Article]
    [Google Scholar]
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