1887

Abstract

The symbiosis , with a worldwide distribution in pantropical and temperate regions, is one of the most studied, because of its potential application as a biofertilizer, especially in rice fields, but also as an animal food and in phytoremediation. The cyanobiont is a filamentous, heterocystic cyanobacterium that inhabits the foliar cavities of the pteridophyte and the indusium on the megasporocarp (female reproductive structure). The classification and phylogeny of the cyanobiont is very controversial: from its morphology, it has been named , , status and recently , but, from its 16S rRNA gene sequence, it has been assigned to and/or , and from its phycocyanin gene sequence, it has been assigned as non- and non-. The literature also points to a possible co-evolution between the cyanobiont and the host, since dendrograms and phylogenetic trees of fatty acids, short tandemly repeated repetitive (STRR) analysis and restriction fragment length polymorphism (RFLP) analysis of genes and the 16S rRNA gene give a two-cluster association that matches the two-section ranking of the host (). Another controversy surrounds the possible existence of more than one genus or more than one species strain. The use of freshly isolated or cultured cyanobionts is an additional problem, since their morphology and protein profiles are different. This review gives an overview of how morphological, chemical and genetic analyses influence the classification and phylogeny of the cyanobiont and future research.

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2014-06-01
2019-12-12
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References

  1. Baker J. A. , Entsch B. , McKay D. B. . ( 2003; ). The cyanobiont in an Azolla fern is neither Anabaena nor Nostoc . . FEMS Microbiol Lett 229:, 43–47. [CrossRef] [PubMed]
    [Google Scholar]
  2. Becking J. H. , Donze M. . ( 1981; ). Pigment distribution and nitrogen fixation in Anabaena azollae . . Plant Soil 61:, 203–226. [CrossRef]
    [Google Scholar]
  3. Bergman B. , Ran L. , Adams D. G. . ( 2008; ). Cyanobacterial-plant symbioses: signalling and development. . In The Cyanobacteria. Molecular Biology, Genomics and Evolution, pp. 447–473. Edited by Herrera A. , Flores E. . . Wymondham, UK:: Caister Academic Press;.
    [Google Scholar]
  4. Carrapiço F. . ( 2010; ). Azolla as a superorganism. Its implication in symbiotic studies. . In Symbioses and Stress (Cellular Origin, Life in Extreme Habitats and Astrobiology, vol. 17) , pp. 225–241. Edited by Seckbach J. , Grube M. . . Amsterdam:: Springer Science+Business Media BV;. [CrossRef]
    [Google Scholar]
  5. Carrapiço F. , Teixeira G. , Diniz M. A. . ( 2000; ). Azolla as a biofertiliser in Africa. A challenge for the future. . Rev Cienc Agric 23:, 120–138.
    [Google Scholar]
  6. Caudales R. , Wells J. M. . ( 1992; ). Differentiation of free-living Anabaena and Nostoc cyanobacteria on the basis of fatty acid composition. . Int J Syst Bacteriol 42:, 246–251. [CrossRef] [PubMed]
    [Google Scholar]
  7. Caudales R. , Wells J. M. , Antoine A. D. . ( 1992; ). Cellular fatty acid composition of symbiotic cyanobacteria isolated from the aquatic fern Azolla . . J Gen Microbiol 138:, 1489–1494. [CrossRef]
    [Google Scholar]
  8. Caudales R. , Wells J. M. , Antoine A. D. , Butterfield J. E. . ( 1995; ). Fatty acid composition of symbiotic cyanobacteria from different host plant (Azolla) species: evidence for coevolution of host and symbiont. . Int J Syst Bacteriol 45:, 364–370. [CrossRef]
    [Google Scholar]
  9. Collinson M. E. . ( 2001; ). Cainozoic ferns and their distribution. . Brittonia 53:, 173–235. [CrossRef]
    [Google Scholar]
  10. Dembitsky V. M. , Shkrob I. , Dor I. . ( 1999; ). Separation and identification of hydrocarbons and other volatile compounds from cultured blue-green alga Nostoc sp. by gas chromatography-mass spectrometry using serially coupled capillary columns with consecutive nonpolar and semipolar stationary phases. . J Chromatogr A 862:, 221–229. [CrossRef] [PubMed]
    [Google Scholar]
  11. Ekman M. , Tollbäck P. , Bergman B. . ( 2008; ). Proteomic analysis of the cyanobacterium of the Azolla symbiosis: identity, adaptation, and nifH modification. . J Exp Bot 59:, 1023–1034. [CrossRef] [PubMed]
    [Google Scholar]
  12. Fjerdingstad E. . ( 1976; ). Anabaena variabilis status azollae . . Arch Hydrobiol (Suppl. 49), 377–381.
    [Google Scholar]
  13. Franche C. , Cohen-Bazire G. . ( 1985; ). The structural nif genes of four symbiotic Anabaena azollae show a highly conserved physical arrangement. . Plant Sci 39:, 125–131. [CrossRef]
    [Google Scholar]
  14. Gates J. E. , Fisher R. W. , Goggin T. W. , Azrolan N. I. . ( 1980; ). Antigenic differences between Anabaena azollae fresh from the Azolla fern leaf cavity and free-living cyanobacteria. . Arch Microbiol 128:, 126–129. [CrossRef]
    [Google Scholar]
  15. Gebhardt J. S. , Nierzwicki-Bauer S. A. . ( 1991; ). Identification of a common cyanobacterial symbiont associated with Azolla spp. through molecular and morphological characterization of free-living and symbiotic cyanobacteria. . Appl Environ Microbiol 57:, 2141–2146.[PubMed]
    [Google Scholar]
  16. Hrouzek P. , Ventura S. , Lukešová A. , Mugnai M. A. , Turicchia S. , Komárek J. . ( 2005; ). Diversity of soil Nostoc strains: phylogenetic and phenotypic variability. . Arch Hydrobiol 159: (Suppl.), 251–264.
    [Google Scholar]
  17. Komárek J. . ( 2005; ). The modern classification of cyanoprokaryotes (cyanobacteria). . Oceanol Hydrobiol Stud 34:, 5–17.
    [Google Scholar]
  18. Komárek J. . ( 2006; ). Cyanobacterial taxonomy: current problems and prospects for the integration of traditional and molecular approaches. . Algae 21:, 349–375. [CrossRef]
    [Google Scholar]
  19. Komárek J. . ( 2010a; ). Modern taxonomy revision of planktic nostocacean cyanobacteria: a short review of genera. . Hydrobiologia 639:, 231–243. [CrossRef]
    [Google Scholar]
  20. 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:, 245–259. [CrossRef]
    [Google Scholar]
  21. Komárek J. , Anagnostidis K. . ( 1989; ). Modern approach to the classification system of cyanophytes. 4. Nostocales. . Arch Hydrobiol 56:, 247–345.
    [Google Scholar]
  22. Ladha J. K. , Watanabe I. . ( 1982; ). Antigenic similarity among Anabaena azollae separated from different species of Azolla . . Biochem Biophys Res Commun 109:, 675–682. [CrossRef] [PubMed]
    [Google Scholar]
  23. Larsson J. , Nylander J. A. A. , Bergman B. . ( 2011; ). Genome fluctuations in cyanobacteria reflect evolutionary, developmental and adaptive traits. . BMC Evol Biol 11:, 187. [CrossRef] [PubMed]
    [Google Scholar]
  24. Lechno-Yossef S. , Nierzwicki-Bauer S. A. . ( 2002; ). Azolla-Anabaena symbiosis. . In Cyanobacteria in Symbiosis, pp. 153–178. Edited by Rai A. N. , Bergman B. , Rasmussen U. . . Dordrecht:: Kluwer;.
    [Google Scholar]
  25. Lumpkin T. A. , Plucknett D. L. . ( 1980; ). Azolla: botany, physiology, and use as a green manure. . Econ Bot 34:, 111–153. [CrossRef]
    [Google Scholar]
  26. Meeks J. C. , Joseph C. M. , Haselkorn R. . ( 1988; ). Organization of the nif genes in cyanobacteria in symbiotic association with Azolla and Anthoceros . . Arch Microbiol 150:, 61–71. [CrossRef] [PubMed]
    [Google Scholar]
  27. Metzgar J. S. , Schneider H. , Pryer K. M. . ( 2007; ). Phylogeny and divergence time estimates for the fern genus Azolla (Salviniaceae). . Int J Plant Sci 168:, 1045–1053. [CrossRef]
    [Google Scholar]
  28. Neumüller M. , Bergman B. . ( 1981; ). The ultrastructure of Anabaena azollae in Azolla pinnata . . Physiol Plant 51:, 69–76. [CrossRef]
    [Google Scholar]
  29. Newton J. W. , Herman A. I. . ( 1979; ). Isolation of cyanobacteria from the aquatic fern, Azolla . . Arch Microbiol 120:, 161–165. [CrossRef]
    [Google Scholar]
  30. Nierzwicki-Bauer S. A. , Haselkorn R. . ( 1986; ). Differences in mRNA levels in Anabaena living freely or in symbiotic association with Azolla . . EMBO J 5:, 29–35.[PubMed]
    [Google Scholar]
  31. Oren A. . ( 2004; ). A proposal for further integration of the cyanobacteria under the Bacteriological Code. . Int J Syst Evol Microbiol 54:, 1895–1902. [CrossRef] [PubMed]
    [Google Scholar]
  32. Oren A. . ( 2011; ). Naming Cyanophyta/Cyanobacteria – a bacteriologist’s view. . Fottea 11:, 9–16.[CrossRef]
    [Google Scholar]
  33. Pabby A. , Prasanna R. , Nayak S. , Singh P. K. . ( 2003; ). Physiological characterization of the cultured and freshly isolated endosymbionts from different species of Azolla . . Plant Physiol Biochem 41:, 73–79. [CrossRef]
    [Google Scholar]
  34. Papaefthimiou D. , Hrouzek P. , Mugnai M. A. , Lukesova A. , Turicchia S. , Rasmussen U. , Ventura S. . ( 2008a; ). Differential patterns of evolution and distribution of the symbiotic behaviour in nostocacean cyanobacteria. . Int J Syst Evol Microbiol 58:, 553–564. [CrossRef] [PubMed]
    [Google Scholar]
  35. Papaefthimiou D. , van Hove C. , Lejeune A. , Rasmussen U. , Wilmotte A. . ( 2008b; ). Diversity and host specificity of Azolla cyanobionts. . J Phycol 44:, 60–70. [CrossRef]
    [Google Scholar]
  36. Pereira A. L. , Figueiredo A. C. , Barroso J. G. , Pedro L. G. , Carrapiço F. . ( 2009; ). Volatile compounds from the symbiotic system Azolla filiculoides-Anabaena azollae-bacteria. . Plant Biosyst 143:, 268–274. [CrossRef]
    [Google Scholar]
  37. Pereira A. L. , Martins M. , Oliveira M. M. , Carrapiço F. . ( 2011; ). Morphological and genetic diversity of the family Azollaceae inferred from vegetative characters and RAPD markers. . Plant Syst Evol 297:, 213–226. [CrossRef]
    [Google Scholar]
  38. Perkins S. K. , Peters G. A. . ( 1993; ). The Azolla-Anabaena symbiosis: endophyte continuity in the Azolla life-cycle is facilitated by epidermal trichomes. I. Partitioning of the endophytic Anabaena into developing sporocarps. . New Phytol 123:, 53–64. [CrossRef]
    [Google Scholar]
  39. Peters G. A. , Mayne B. C. . ( 1974; ). The Azolla, Anabaena azollae relationship. I. Initial characterization of the association. . Plant Physiol 53:, 813–819. [CrossRef] [PubMed]
    [Google Scholar]
  40. Peters G. A. , Perkins S. K. . ( 1993; ). The Azolla-Anabaena symbiosis: endophyte continuity in the Azolla life-cycle is facilitated by epidermal trichomes. II. Re-establishment of the symbiosis following gametogenesis and embryogenesis. . New Phytol 123:, 65–75. [CrossRef]
    [Google Scholar]
  41. Peters G. A. , Calvert H. E. , Kaplan D. , Ito O. , Toia R. E. Jr . ( 1982; ). The Azolla-Anabaena symbiosis: morphology, physiology and use. . Isr J Bot 31:, 305–323.
    [Google Scholar]
  42. Plazinski J. , Zheng Q. , Taylor R. , Croft L. , Rolfe B. G. , Gunning B. E. S. . ( 1990; ). DNA probes show genetic variation in cyanobacterial symbionts of the Azolla fern and a closer relationship to free-living Nostoc strains than to free-living Anabaena strains. . Appl Environ Microbiol 56:, 1263–1270.[PubMed]
    [Google Scholar]
  43. Rajaniemi P. , Hrouzek P. , Kastovská 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). . Int J Syst Evol Microbiol 55:, 11–26. [CrossRef] [PubMed]
    [Google Scholar]
  44. Ran L. , Larsson J. , Vigil-Stenman T. , Nylander J. A. A. , Ininbergs K. , Zheng W.-W. , Lapidus A. , Lowry S. , Haselkorn R. , Bergman B. . ( 2010; ). Genome erosion in a nitrogen-fixing vertically transmitted endosymbiotic multicellular cyanobacterium. . PLoS ONE 5:, e11486. [CrossRef] [PubMed]
    [Google Scholar]
  45. Reid J. D. , Plunkett G. M. , Peters G. A. . ( 2006; ). Phylogenetic relationships in the heterosporous fern genus Azolla (Azollaceae) based on DNA sequence data from noncoding regions. . Int J Plant Sci 167:, 529–538. [CrossRef]
    [Google Scholar]
  46. Shi D.-J. , Hall D. O. . ( 1988; ). The Azolla-Anabaena association: historical perspective, symbiosis and energy metabolism. . Bot Rev 54:, 353–386. [CrossRef]
    [Google Scholar]
  47. Sood A. , Prasanna R. , Prasanna B. M. , Singh P. K. . ( 2008a; ). Genetic diversity among and within cultured cyanobionts of diverse species of Azolla . . Folia Microbiol (Praha) 53:, 35–43. [CrossRef] [PubMed]
    [Google Scholar]
  48. Sood A. , Prasanna R. , Singh P. K. . ( 2008b; ). Fingerprinting of freshly separated and cultured cyanobionts from different Azolla species using morphological and molecular markers. . Aquat Bot 88:, 142–147. [CrossRef]
    [Google Scholar]
  49. Strasburger E. . ( 1873; ). Über Azolla. Leipzig:: Verlag von Ambr. Abel;.
    [Google Scholar]
  50. Strasburger E. . ( 1884; ). Das Botanische Practicum. Jena & Leipzig:: Gustav Fischer;.
    [Google Scholar]
  51. Svenning M. M. , Eriksson T. , Rasmussen U. . ( 2005; ). Phylogeny of symbiotic cyanobacteria within the genus Nostoc based on 16S rDNA sequence analyses. . Arch Microbiol 183:, 19–26. [CrossRef] [PubMed]
    [Google Scholar]
  52. Tang L. F. , Watanabe I. , Liu C. C. . ( 1990; ). Limited multiplication of symbiotic cyanobacteria of Azolla spp. on artificial media. . Appl Environ Microbiol 56:, 3623–3626.[PubMed]
    [Google Scholar]
  53. Van Coppenolle B. , McCouch S. R. , Watanabe I. , Huang N. , Van Hove C. . ( 1995; ). Genetic diversity and phylogeny analysis of Anabaena azollae based on RFLPs detected in Azolla-Anabaena azollae DNA complexes using nif gene probes. . Theor Appl Genet 91:, 589–597.[PubMed] [CrossRef]
    [Google Scholar]
  54. Wagner G. M. . ( 1997; ). Azolla: a review of its biology and utilization. . Bot Rev 63:, 1–26. [CrossRef]
    [Google Scholar]
  55. Zheng W. W. , Nilsson M. , Bergman B. , Rasmussen U. . ( 1999; ). Genetic diversity and classification of cyanobacteria in different Azolla species by the use of PCR fingerprinting. . Theor Appl Genet 99:, 1187–1193. [CrossRef]
    [Google Scholar]
  56. Zheng W. , Bergman B. , Chen B. , Zheng S. , Guan X. , Rasmussen U. . ( 2009; ). Cellular responses in the cyanobacterial symbiont during its vertical transfer between plant generations in the Azolla microphylla symbiosis. . New Phytol 181:, 53–61. [CrossRef] [PubMed]
    [Google Scholar]
  57. Zimmerman W. J. , Rosen B. H. , Lumpkin T. A. . ( 1989; ). Enzymatic, lectin, and morphological characterization and classification of presumptive cyanobionts from Azolla Lam.. New Phytol 113:, 497–503. [CrossRef]
    [Google Scholar]
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