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Azolla as a Superorganism. Its Implication in Symbiotic Studies

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Book cover Symbioses and Stress

Part of the book series: Cellular Origin, Life in Extreme Habitats and Astrobiology ((COLE,volume 17))

Abstract

The symbiosis history begun many million years ago, probably even before the first manifestation of life arose in our planet (Carrapiço et al., 2007). But it was only in the nineteenth century with the presentation in 1867, by the Swiss botanist Simon Schwendener, of the “dual hypothesis” related to the lichens structure, that this “real story” had a scientific starting point for society (Boucher, 1985; Sapp, 1994; Honegger, 2000).

This article is dedicated to Prof. Maria Grilli Caiola life’s work and her contribution to the construction and development of the modern symbiotic studies, namely on the Azolla-Anabaena bacteria research.

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Notes

  1. 1.

    This article is dedicated to Prof. Maria Grilli Caiola life’s work and her contribution to the construction and development of the modern symbiotic studies, namely on the Azolla-Anabaena-bacteria research.

References

  • Adams, D.G. (2000) Symbiotic interactions, In: B.A. Whitton and M. Potts (eds.) The Ecology of Cyanobacteria. Their Diversity in Time and Space. Kluwer Academic Press, London, pp. 523–561.

    Google Scholar 

  • Becking, J.H. (1987) Endophyte transmission and activity in the Anabaena-Azolla association. Plant Soil 100: 183–212.

    Article  Google Scholar 

  • Bouchard, F. (2007) What is a symbiotic superorganism and how do you measure its fitness? Abstracts of the ISHPSSB Meeting, University of Exeter, Devon, UK, July 25−29, p. 45.

    Google Scholar 

  • Boucher, D.H. (ed.) (1985) The biology of mutualism. Ecology and Evolution. Oxford University Press, New York.

    Google Scholar 

  • Braun-Howland, E.B. and Nierzwicki-Bauer, S.A. (1990) Azolla-Anabaena symbiosis: biochemistry, physiology, ultrastructure, and molecular biology, In: A.N. Rai (ed.) CRC Handbook of Symbiotic Cyanobacteria. CRC Press, Boca Raton, FL, pp. 65–117.

    Google Scholar 

  • Brinkhuis et al. (2006) Episodic fresh surface waters in the Eocene Arctic Ocean. Nature 441: 606–609.

    Article  PubMed  CAS  Google Scholar 

  • Bujak, J. (2007) The Azolla story. Climate change and Arctic hydrocarbons. GEO ExPro September 4 (4): 66–72.

    Google Scholar 

  • Canini, A., Bergman, B., Civitareale, P., Rotilio, G. and Grilli Caiola, M. (1992) Localization of iron-superoxide dismutase in the cyanobiont of Azolla filiculoides Lam. Protoplasma 169: 1–8.

    Article  Google Scholar 

  • Carrapiço, F. (1991) Are bacteria the third partner of the Azolla-Anabaena Symbiosis? Plant Soil 137: 157–160.

    Article  Google Scholar 

  • Carrapiço, F. (2002) The Azolla-Anabaena-Bacteria system as a natural microcosm. Proc. SPIE 4495: 261–265.

    Article  Google Scholar 

  • Carrapiço, F., Costa, M.H., Costa, M.L., Teixeira, G., Frazão, A.A., Santos, M.C.R. and Baioa, M.V. (1996) The uncontrolled growth of Azolla in the Guadiana River. Aquaphyte 16(2): 11.

    Google Scholar 

  • Carrapiço, F., Teixeira, G. and Diniz, M.A. (2000) Azolla as biofertiliser in Africa. A challenge for the future. Revista de Ciências Agrárias 23(3–4): 120–138.

    Google Scholar 

  • Carrapiço, F., Pereira, L. and Rodrigues, T. (2007) Contribution to a symbiogenic approach in astrobiology. Proc. SPIE 6694: 669406-1–669406–10.

    Article  Google Scholar 

  • Collinson, M.E., Barke, J., van der Burgh, J. and van Konijnenburg-van Cittert, J.H.A. (2009) A new species of the freshwater fern Azolla (Azollaceae) from the Eocene Arctic Ocean. Rev. Palaeobot. Palynol. 155: 1–14.

    Google Scholar 

  • Costa, M.L., Santos, M.C.R. and Carrapiço, F. (1999) Biomass characterization of Azolla filiculoides grown in natural ecosystems and wastewater. Hydrobiologia 415: 323–327.

    Article  Google Scholar 

  • De Bary, A. (1878) Ueber Symbiose. – Tageblatt 51. Versamml. Deutscher Naturforscher u. Aerzte, Cassel 1878: 121–126.

    Google Scholar 

  • De Bary, A. (1879) Die Erscheinung der Symbiose. Vortrag auf der Versammlung der Deutschen Naturforscher und Aertze zu Cassel. Verlag von Karl J. Trubner, Strasburg, pp. 1–30.

    Google Scholar 

  • Douglas, A.E. (1994) Symbiotic Interactions. Oxford University Press, Oxford.

    Google Scholar 

  • Dubos, R. and Kessler, A. (1963) Integrative and disintegrative factors in symbiotic associations, In: P.S. Nutman and B. Mosse (eds.) Proceedings of the Thirteenth Symposium of the Society for General Microbiology. London, pp. 1–11.

    Google Scholar 

  • Ekman, M., Tollback, P and Bergman, B. (2008) Proteomic analysis of the cyanobacterium of the Azolla symbiosis: identity, adaptation, and NifH modification. J. Exp. Bot. 59(5): 1023–1034.

    Article  PubMed  CAS  Google Scholar 

  • Evrard, C. and Van Hove, C. (2004) Taxonomical of the American Azolla species (Azollaceae). A critical review. Syst. Geogr. Pl. 74: 301–318.

    Google Scholar 

  • Feuillée, L. (1725) Journal des observations physiques, mathematiques et botaniques, faites par ordre du roi sur les côtes orientales de l’Amerique Meridionale, & aux Indes Occidentales et dans un autre voyage faite par le même ordre à la nouvelle Espagne, & aux Illes de l’Amerique. Jean Mariette, Paris.

    Google Scholar 

  • Forni, C., Chen, J., Tancioni, L. and Caiola, M.G. (2001) Evaluation of fern Azolla for growth, nitrogen and phophorus removal from wastewater. Water Res. 35(6): 1592–1598.

    Article  PubMed  CAS  Google Scholar 

  • Frank, A.B. (1877) Ueber die biologischen Verhältnisse des Thallus einiger Krustenflechten. Beitr. Biol. Pfl. 2(2): 123–200.

    Google Scholar 

  • Grilli, M. (1964) Infrastrutture di Anabaena azollae vivente nelle foglioline di Azolla caroliniana. Ann. Microb. Enzim. 14: 69–90.

    Google Scholar 

  • Grilli Caiola, M. and Forni, C. (1999) The hard life of prokaryotes in the leaf cavities of Azolla, In: J. Seckbach (ed.) Enigmatic Microorganisms and Life in Extreme Environments. Kluwer Academic, Dordrecht, The Netherlands, pp. 629–639.

    Chapter  Google Scholar 

  • Honegger, R. (2000) Simon Schwendener (1829–1919) and the dual hypothesis of lichens. Bryologist 103: 167–183.

    Article  Google Scholar 

  • Lamarck, J-B. (1783) Azolla filiculoides. Encyclopédie Méthodique: Botanique. Tome 1: 343, Paris.

    Google Scholar 

  • Lechno-Yossef, S. and Nierzwicki-Bauer, S.A. (2002) Azolla-Anabaena symbiosis, In: A.N. Rai, B. Bergman and U. Rasmussen (eds.) Cyanobacteria in Symbiosis. Kluwer, Dordrecht, pp. 153−178.

    Google Scholar 

  • Lindblad, P., Bergman, B. and Nierzwicki-Bauer, S.A. (1991) Immunocytochemical localization of nitrogenase in bacteria symbiotically associated with Azolla spp, Appl. Environ. Microbiol. 57: 3637–3640.

    PubMed  CAS  Google Scholar 

  • Lumpkin, T.A. (1993) Azollaceae Wettstein. Azolla Family. Flora N. Am. 2: 338–342.

    Google Scholar 

  • Monnier, J., Lavondes, A., Jolinon, J-C. and Elouard, P. (1993), In: Association Saint-Guignefort (ed.) Philibert Commerson. Le découvreur du bougainvillier. Châtillon-sur-Chalaronne, France.

    Google Scholar 

  • Papaefthimiou, D., Van Hove, C., Lejeune, A., Rasmussen, U. and Wilmotte, A. (2008) Diversity and host specificity of Azolla cyanobionts. J. Phycol. 44: 60–70.

    Article  CAS  Google Scholar 

  • Pereira, A.L. and Carrapiço, F. (2007) Histochemistry of simple hairs from the foliar cavities of Azolla filiculoides. Plant Biosys. 141: 323–328.

    Article  Google Scholar 

  • Peters, G.A. and Meeks, J.C. (1989) The Azolla-Anabaena symbiosis: basic biology. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40: 193–210.

    Article  Google Scholar 

  • Rai, V., Sharma, N.K., and RTai, A.K. (2006) Growth and cellular ion content of salt-sensitive symbiotic system Azolla pinnata-Anabaena azollae under NaCl stress. J. Plant Physiol. 163: 937–944.

    Article  PubMed  CAS  Google Scholar 

  • Sapp, J. (1994) Evolution by association. A History of Symbiosis. Oxford University Press, New York.

    Google Scholar 

  • Sapp, J. (2003) Genesis: The evolution of biology. Oxford University Press, New York.

    Google Scholar 

  • Sapp, J., Carrapiço, F. and Zolotonodov, M. (2002) Symbiogenesis: the hidden face of Constantin Merezhkowsky. Hist. Phil. Life Sci. 24: 421–449.

    Google Scholar 

  • Schiebinger, L. (2003) Jeanne Barret: the first woman to circumnavigate the globe. Endeavour 27(1): 22–25.

    Article  PubMed  Google Scholar 

  • Seckback, J. (ed.) (2002) Symbiosis: Mechanisms and Model Systems. Kluwer Academic, Dordrecht, The Netherlands.

    Google Scholar 

  • Serrano, R., Carrapiço, F. and Vidal, R. (1999) The presence of lectins in bacteria associated with the Azolla-Anabaena symbiosis. Symbiosis 27: 169–178.

    Google Scholar 

  • Shi, D.J. and Hall, D.O. (1988) Azolla and immobilized cyanobacteria (blue-green algae): from traditional agriculture to biotechnology. Plants Today 1: 5−12.

    Google Scholar 

  • Strasburger, E. (1873) Uber Azolla. Herman Dabis Verlag, Jena.

    Google Scholar 

  • Svenson, H.K. (1944) The new world species of Azolla. Am. Fern. J. 34: 69–84.

    Article  Google Scholar 

  • Tung, H.F. and Watanabe, I. (1983) Differential response of Azolla-Anabaena associations to high temperature and minus phosphorus treatments. New Phytol. 93: 423–431.

    Article  CAS  Google Scholar 

  • Uheda, E. (1986) Isolation of hair cells from Azolla filiculoides var. japonica Leaves. Plant Cell Physiol. 27: 1255–1261.

    CAS  Google Scholar 

  • Veys, P., Waterkeyn L, Lejeune, A., Van Hove, C. (1999) The pore of the leaf cavity of Azolla: morphology, cytochemistry and possible functions. Symbiosis 27: 33–57.

    Google Scholar 

  • Zook, D. (1998) A new symbiosis language, ISS Symbiosis News March 1998, 1 (3): 1–3.

    Google Scholar 

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Acknowledgments

The author is grateful and expresses his sincere thanks to Dr. Frédéric Danet, Head of the Herbarium of the Botanical Garden of Lyon (LYJB), France, for the photos and information about the Azolla samples existing at the LYJB, and to Dr. Cécile Aupic, Dr. Gérard Aymonin, and Dr. Germinal Rouhan, from the Herbarium of the Muséum National d’Histoire Naturel of Paris, for the facilities to study the historical Azolla samples existing in their Institution. A special thanks to Dr. Jeannine Monnier for the information on Philibert Commerson’s life and work and to Dr. Jonathan Bujak for the discussion and comments on the ACEX material and Azolla found in the Arctic, and to Dr. Ana L. Pereira for the research work developed on the biology of Azolla for her Ph.D. thesis. A particular thanks to the anonymous referee for the comments and suggestions and to Helena Carrapiço for the English revision of the manuscript.

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  1. Faculty of Science, Department of Plant Biology, Centre for Environmental Biology, University of Lisbon, Bloco C2, Campo Grande, 1749–016, Lisboa, Portugal

    Francisco Carrapiço

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Correspondence to Francisco Carrapiço .

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  1. University of Jerusalem, Mevo Hadas 20, Efrat, 90435, Israel

    Joseph Seckbach

  2. , Institute of Plant Sciences, Karl-Franzens-University, Holteigasse 6, Graz, 8010, Austria

    Martin Grube

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Carrapiço, F. (2010). Azolla as a Superorganism. Its Implication in Symbiotic Studies. In: Seckbach, J., Grube, M. (eds) Symbioses and Stress. Cellular Origin, Life in Extreme Habitats and Astrobiology, vol 17. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-9449-0_11

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