Light micrograph of Anabaena azollae strain 0708. The filaments are composed of photosynthetic vegetative cells and nitrogen-fixing heterocysts (the spaced larger cells). Scale bar = 50 μm.
Electron microscopy micrograph of part of a filament from Anabaena azollae strain 0708. The larger heterocyst is flanked by vegetative cells.
This organism is now known as 'Nostoc azollae' 0708, (9/12/08).
Anabaena azollae strain 0708 is a cyanobacterium living in symbiosis with the free-floating water-fern Azolla filiculoides (Division: Pteridophyta; Order: Salviniales; Family: Azollaceae Wettst.; Genus: Azolla Lam.). The cyanobacterium in Azolla (the cyanobiont) belongs to the photoautotrophic filamentous type of cyanobacteria (Section IV) that are capable of oxygenic photosynthesis and CO2 capture, as well as nitrogen fixation (see Adams et al. 2005; Bergman et al. 2008).
The Azolla cyanobiont produce combined nitrogen, and as a side-reaction, the nitrogen-fixing enzyme also produces hydrogen gas, a potentially important bio-gas (Lechno-Yossef & Nierzwicki-Bauer 2002; van Hove & Lejune 2002). These features, combined with a fast growth using solar energy only, make biomass production and energy conversions (e.g. into bio-fuels) via the Azolla symbiosis energetically attractive.
The cyanobiont of Azolla is taxonomically well rooted close to the nitrogen-fixing genera Nostoc and Anabaena (Svenning et al. 2005, Ekman et al. 2007). The cyanobiont of Azolla has a flexible life style including symbiotic competence and ability to differentiate several cell types from the photosynthetic vegetative cells: hormogonia (short, small-celled and motile filaments), nitrogen-fixing heterocysts and resting akinetes (spores), all cell-types seen in the Azolla symbiosis (Zheng et al. 2008).
The Azolla host is a heterosporous fern (genome size of about 720 Mb) and represents a wide-spread and fast-growing plant with a doubling time of 2-5 days (van Hove & Lejune 2002).Seven species are recognized. The cyanobacteria colonize ‘cavities’ found in all dorsal leaves of the Azolla plant (Lechno-Yossef & Nierzwicki-Bauer 2002). The plant supplies the cyanobiont with fixed carbon, and receives a perpetual source of combined ‘new’ nitrogen from the nitrogen-fixing cyanobiont (Meeks et al. 1988). The Azolla cyanobiont also shows unique characters. For instance, the cyanobiont is vertically transmitted into new plant generations within the plant reproductive organs, the sporocarps (Perkins & Peters 1993; Zheng et al. 2008). Also, the cyanobiont seems to have lost its capacity for independent growth (Lechno-Yossef & Nierzwicki-Bauer 2002). We therefore hypothesize that Azolla is evolutionarily the most advanced extant plant symbiosis and potentially on its way to develop into a plant with a nitrogen-fixing ‘organelle’.
The Azolla symbiosis has been used to sustain agricultural productivity in south-east Asia for over a thousand years (van Hove & Lejune 2002). The symbiosis is involved in vital processes such as energy capture and production of energy rich carbohydrates via photosynthesis (carbon sequestration) and combined nitrogen fixation (nitrogen sequestration), processes fed by solar energy. The Azolla symbiosis thereby represents a most self-renewable source of energy and key nutrients. An understanding of the cyanobacterial genome may open new perspectives for biotechnological innovation related to the production of N-fertilizers and bio-energy conversions and may help alleviate our dependence on industrially and oil-based nitrogen. It will also provide information in exciting areas of biology, notably in evolution and inter-kingdom interactions.
Adams DG, Bergman B, Nierzwicki-Bauer SA, Rai AN & Schüssler A 2006. Cyanobacterial-Plant Symbioses. In: M Dworkin, S Falkow, E Rosenberg, KH Schleifer & E. Stackebrandt (Eds.) The Prokaryotes. A Handbook on the Biology of Bacteria, Third edition. Vol. 1: Symbiotic Associations, Biotechnology, Applied Microbiology, Springer, New York, pp. 331-363.
Bergman B, Ran L & Adams DA 2008. Cyanobacterial-plant symbioses: signalling and development. In: A Herrero & E Flores (Eds.) The Cyanobacteria: Molecular Biology, Genomics and Evolution. Caister Academic Press. pp. 447-473. ISBN: 978-1-904455-15-8.
Ekman M, Tollbäck P & Bergman B 2008. Proteomic analyses of the cyanobacterium of the Azolla symbiosis: identification, adaptation and NifH modification. J. Exp. Bot. 59, 1023-34.
Lechno-Yossef S & Nierzwicki-Bauer SA 2002. Azolla-Anabaena symbiosis. In: AN Rai, B Bergman & U Rasmussen (Eds.) Cyanobacteria in Symbiosis. Dordrecht, The Netherlands: Kluwer Academic Publishers, 153-178.
Meeks JC, Joseph CM & Haselkorn R 1988. Organization of the nif genes in cyanobacteria in symbiotic association with Azolla and Anthoceros. Arch Microbiol 15, 61-71.
Perkins SK & Peters GA 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 Phytologist 123, 53-64.
Svenning MM, Eriksson T & Rasmussen U 2005. Phylogeny of symbiotic cyanobacteria within the genus Nostoc based on 16S rDNA sequence analyses. Arch Microbiol. 183, 19-26.
Usher K, Bergman B & Raven J 2007. Exploring cyanobacterial mutualisms. Ann. Rev. Ecol. Evol. Syst. 38, 255-273.
van Hove C & Lejeune A 2002. Applied aspects of Azolla-Anabaena symbiosis. In: AN Rai, B Bergman & U Rasmussen (Eds.) Cyanobacteria in Symbiosis. Dordrecht, The Netherlands: Kluwer Academic Publishers, 117-135.
Zheng WW, Bergman B & Rasmussen U 2008. Cyanobacteria in developing sporocarps of the water fern Azolla: cell differentiation, vesicle liberation and biofilm formation. New Phytol. (in press).