1887

Abstract

Many cyanobacteria commonly identified as belonging to the genus are well-known cyanobionts (symbionts) of a wide variety of plants and fungi. They form symbioses with bryophytes, pteridophytes, gymnosperms and angiosperms that are considerably different in the type of reciprocal interaction between the host and the cyanobiont. The phylogenetic and taxonomic relationships among cyanobionts isolated from different hosts and strains isolated from free-living conditions are still not well understood. We compared phylogeny and morphology of symbiotic cyanobacteria originating from different host plants (genera , , , , , and ) with free-living isolates originating from different habitats. After preliminary clustering with ARDRA (amplified rDNA restriction analysis), phylogeny was reconstructed on the basis of 16S rRNA gene sequences and compared with morphological characterization, obtaining several supported clusters. Two main clusters harboured almost all cyanobionts of , and of several cycads, together with free-living strains of the species , , , and strains related to . We suggest that the frequent occurrence of symbiotic strains within these clusters is explained by the intensive hormogonia production that was observed in many of the strains studied. However, no evidence for discrimination between symbiotic and free-living strains, either by molecular or morphological approaches, could be found. Sequences of cyanobiont filaments, taken directly from leaf cavities, clustered tightly with sequences from the planktic cyanobacterium , from the benthic 133 and from HINDAK 1984/43, with high bootstrap values. The phylogenetic analysis showed that two distinct patterns of evolution of symbiotic behaviour might exist for the nostocacean cyanobacteria, one leading to symbioses of species with a wide variety of plants, the other leading to the association of a unique cyanobacterial type with the water fern .

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2008-03-01
2024-03-28
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References

  1. Anagnostidis, K. & Kómarek, J.(1988). Modern approach to the classification system of cyanophytes 3 – Oscillatoriales. Arch Hydrobiol Suppl 80, 327–472. [Google Scholar]
  2. 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] [Google Scholar]
  3. 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 co-evolution of host and symbiont. Int J Syst Bacteriol 45, 364–370.[CrossRef] [Google Scholar]
  4. Costa, J.-L., Paulsrud, P. & Lindblad, P.(1999). Cyanobiont diversity within coralloid roots of selected cycad species. FEMS Microbiol Ecol 28, 85–91.[CrossRef] [Google Scholar]
  5. Costa, J. L., Paulsrud, P. & Lindblad, P.(2001). Genetic diversity of Nostoc symbionts endophytically associated with two bryophyte species. Appl Environ Microbiol 67, 4393–4396.[CrossRef] [Google Scholar]
  6. Fiore, M. de F., Neilan, B. A., Copp, J. N., Rodrigues, J. L. M., Tsai, S. M., Lee, H. & Trevors, J. T.(2005). Characterization of nitrogen-fixing cyanobacteria in the Brazilian Amazon floodplain. Water Res 39, 5017–5026.[CrossRef] [Google Scholar]
  7. 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. [Google Scholar]
  8. Gordon, D.(2004). Viewing and editing assembled sequences using Consed. In Current Protocols in Bioinformatics, pp. 11.2.1–11.2.43. Edited by A. D. Baxevanis & D. B. Davison. New York: Wiley.
  9. Guevara, R., Armesto, J. J. & Caru, M.(2002). Genetic diversity of Nostoc microsymbionts from Gunnera tinctoria revealed by PCR-STRR fingerprinting. Microb Ecol 44, 127–136.[CrossRef] [Google Scholar]
  10. Gugger, M., Lyra, C., Henriksen, P., Couté, A., Humbert, J.-F. & Sivonen, K.(2002). Phylogenetic comparison of the cyanobacterial genera Anabaena and Aphanizomenon. Int J Syst Evol Microbiol 52, 1867–1880.[CrossRef] [Google Scholar]
  11. Henson, B. J., Watson, L. E. & Barnum, S. R.(2002). Molecular differentiation of the heterocystous cyanobacteria, Nostoc and Anabaena, based on complete nifD sequences. Curr Microbiol 45, 161–164.[CrossRef] [Google Scholar]
  12. Henson, B. J., Hesselbrock, S. M., Watson, L. E. & Barnum, S. R.(2004). Molecular phylogeny of the heterocystous cyanobacteria (subsections IV and V) based on nifD. Int J Syst Evol Microbiol 54, 493–497.[CrossRef] [Google Scholar]
  13. Hill, D. J.(1975). The pattern of development of Anabaena in the Azolla-Anabaena symbiosis. Planta 122, 179–184.[CrossRef] [Google Scholar]
  14. Hrouzek, P., Simek, M. & Komárek, J.(2003). Nitrogenase activity (acetylene reduction activity) and diversity of six soil Nostoc strains. Arch Hydrobiol Suppl 146, 87–101. [Google Scholar]
  15. 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 Suppl 159, 251–264. [Google Scholar]
  16. Komárek, J. & Anagnostidis, K.(1989). Modern approach to the classification system of cyanophytes 4 – Nostocales. Arch Hydrobiol Suppl 82, 247–345. [Google Scholar]
  17. Lachance, M.-A.(1981). Genetic relatedness of heterocystous cyanobacteria by deoxyribonucleic acid-deoxyribonucleic acid reassociation. Int J Syst Bacteriol 31, 139–147.[CrossRef] [Google Scholar]
  18. Lazaroff, N.(1966). Photoinduction and photoreversal of the Nostocacean developmental cycle. J Phycol 2, 7–17.[CrossRef] [Google Scholar]
  19. Lazaroff, N. & Vishniac, W.(1961). The effect of light on the developmental cycle of Nostoc muscorum, a filamentous blue-green alga. J Gen Microbiol 25, 365–374.[CrossRef] [Google Scholar]
  20. Lechno-Yossef, S. & Nierzwicki-Bauer, S. A.(2002).Azolla-Anabaena symbiosis. In Cyanobacteria in Symbiosis, pp. 153–178. Edited by A. N. Rai, B. Bergman & U. Rasmussen. Dordrecht: Kluwer Academic.
  21. Lohtander, K., Oksanen, I. & Rikkinen, J.(2003). Genetic diversity of green algal and cyanobacterial photobionts in Nephroma (Peltigerales). Lichenologist 35, 325–339.[CrossRef] [Google Scholar]
  22. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, Buchner, A., Lai, T., Steppi, S. & other authors(2004).arb: a software environment for sequence data. Nucleic Acids Res 32, 1363–1371.[CrossRef] [Google Scholar]
  23. Mollenhauer, D.(1970). Beiträge zur Kenntnis der Gattung Nostoc. Abh Senckenb Naturf Ges 524, 1–80. [Google Scholar]
  24. Nilsson, M., Bergman, B. & Rasmussen, U.(2000). Cyanobacterial diversity in geographically related and distant host plants of the genus Gunnera. Arch Microbiol 173, 97–102.[CrossRef] [Google Scholar]
  25. 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]
  26. Papaefthimiou, D., Van Hove, C., Lejeune, A., Rasmussen, U. & Wilmotte, A.(2008). Diversity and host specificity of genus Azolla cyanobionts. J Phycol in press [Google Scholar]
  27. Peters, G. A. & Mayne, B. C.(1974). The Azolla, Anabaena azollae relationship. I. Initial characterisation of the association. Plant Physiol 53, 813–819.[CrossRef] [Google Scholar]
  28. 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. [Google Scholar]
  29. Rai, A. N., Söderbäck, E. & Bergman, B.(2000). Tansley review no. 116. Cyanobacterium–plant symbioses. New Phytol 147, 449–481.[CrossRef] [Google Scholar]
  30. Rai, H., Bergman, B. & Rasmussen, U.(2002).Cyanobacteria in Symbiosis. Dordrecht: Kluwer Academic.
  31. Rajaniemi, P., Hrouzek, P., Kastovská, K., Willame, R., Rantala, A., Hoffman, 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] [Google Scholar]
  32. Rasmussen, U. & Nilsson, M.(2002). Cyanobacterial diversity and specificity in plant symbioses. In Cyanobacteria in Symbiosis, pp. 313–328. Edited by A. N. Rai, B. Bergman & U. Rasmussen. Dordrecht: Kluwer Academic.
  33. Rasmussen, U. & Svenning, M. M.(1998). Fingerprinting of cyanobacteria based on PCR with primers derived from short and long tandemly repeated repetitive sequences. Appl Environ Microbiol 64, 265–272. [Google Scholar]
  34. Rikkinen, J., Oksanen, I. & Lohtander, K.(2002). Lichen guilds share related cyanobacterial symbionts. Science 297, 357[CrossRef] [Google Scholar]
  35. Rippka, R. & Herdman, M.(1992).Catalogue of strains. Pasteur culture collection of cyanobacterial strains in axenic culture. Paris, France: Institute Pasteur.
  36. Rippka, R., Deruelles, J., Waterbury, J. B., Herdman, M. & Stanier, R. Y.(1979). Generic assignments, strain histories, and properties of pure cultures of cyanobacteria. J Gen Microbiol 111, 1–61.[CrossRef] [Google Scholar]
  37. Rippka, R., Castenholz, R. W. & Herdman, M.(2001). Subsection IV. (Formerly Nostocales Castenholz 1989b sensu Rippka, Deruelles, Waterbury, Herdman and Stanier 1979). In Bergey's Manual of Systematic Bacteriology, 2nd edn, vol. 1, pp. 562–589. Edited by D. R. Boone, R. W. Castenholz & G. M. Garrity. New York: Springer.
  38. Scheldeman, P., Baurain, D., Bouhy, R., Scott, M., Mühling, M., Whitton, B. A., Belay, A. & Wilmotte, A.(1999).Arthrospira (‘Spirulina’) strains from four continents are resolved into only two clusters, based on amplified ribosomal DNA restriction analysis of the internally transcribed spacer. FEMS Microbiol Lett 172, 213–222.[CrossRef] [Google Scholar]
  39. Strasburger, E.(1884). Die Controversen der indirecten Keimtheilung. Arch Mikrob Anat 23, 301 (in German). [Google Scholar]
  40. 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] [Google Scholar]
  41. Taton, A., Grubisic, S., Brambilla, E., De Wit, R. & Wilmotte, A.(2003). Cyanobacterial diversity in natural and artificial microbial mats of Lake Fryxell (McMurdo Dry Valleys, Antarctica): a morphological and molecular approach. Appl Environ Microbiol 69, 5157–5169.[CrossRef] [Google Scholar]
  42. Tomaselli, L., Margheri, M. C., Giovannetti, L., Sili, C. & Carlozzi, P.(1988). The taxonomy of Azolla spp. cyanobionts. Ann Microbiol 38, 157–161. [Google Scholar]
  43. Vagnoli, L., Margheri, M. C., Allotta, G. & Materassi, R.(1992). Morphological and physiological properties of symbiotic cyanobacteria. New Phytol 120, 243–249.[CrossRef] [Google Scholar]
  44. van Hove, C. & Lejeune, A.(2002). Applied aspects of Azolla-Anabaena symbiosis. In Cyanobacteria in Symbiosis, pp. 179–193. Edited by A. N. Rai, B. Bergman & U. Rasmussen. Dordrecht: Kluwer Academic.
  45. West, N. J. & Adams, D. G.(1997). Phenotypic and genotypic comparison of symbiotic and free-living cyanobacteria. Appl Environ Microbiol 63, 4479–4484. [Google Scholar]
  46. 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]
  47. Zheng, W., Song, T., Bao, X., Bergman, B. & Rasmussen, U.(2002). High cyanobacterial diversity in coralloid roots of cycads revealed by PCR fingerprinting. FEMS Microbiol Ecol 40, 215–222.[CrossRef] [Google Scholar]
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vol. , part 3, pp. 553–564

Amplified rDNA restriction analysis (ARDRA) of symbiotic and free-living cyanobacteria performed on the 16S rRNA gene+ITS region. [PDF](21 KB)



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