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Differential patterns of evolution and distribution of the symbiotic behaviour in nostocacean cyanobacteria

¹ Department of Botany, Stockholm University, S-10691 Stockholm, Sweden
² Department of Botany, Faculty of Biological Sciences, University of South Bohemia, eské Budjovice, Czech Republic
³ Institute of Physical Biology, University of South Bohemia, Nové Hrady, Czech Republic
⁴ Institute of Microbiology, Department of Autotrophic Microorganisms, Academy of Sciences of the Czech Rrepublic, Opatovick Mln, Tebo, Czech Republic
⁵ Institute of Ecosystem Study, National Research Council of Italy, via Madonna del Piano 10, 50019 Sesto Fiorentino, Italy
⁶ PhD School in Science for Conservation of the Cultural Heritage, University of Florence, Italy
⁷ Institute of Soil Biology, Biology Centre AS CR, v. v. i., Na Sádkách 7, 37005 eské Budjovice, Czech Republic
⁸ PhD School in Polar Science, University of Siena, Italy

Correspondence
Stefano Ventura
stefano.ventura{at}ise.cnr.it

Many cyanobacteria commonly identified as belonging to the genus Nostoc 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 Nostoc 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 Gunnera, Azolla, Cycas, Dioon, Encephalartos, Macrozamia and Anthoceros) with free-living Nostoc 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 Nostoc clusters harboured almost all cyanobionts of Gunnera, Anthoceros and of several cycads, together with free-living strains of the species Nostoc muscorum, Nostoc calcicola, Nostoc edaphicum, Nostoc ellipsosporum and strains related to Nostoc commune. 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 Azolla cyanobiont filaments, taken directly from leaf cavities, clustered tightly with sequences from the planktic cyanobacterium Cylindrospermopsis raciborskii, from the benthic Anabaena cylindrica 133 and from Anabaena oscillarioides 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 Nostoc species with a wide variety of plants, the other leading to the association of a unique cyanobacterial type with the water fern Azolla.

The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences determined in this study are AM711522–AM711554.

A supplementary figure showing the ARDRA of symbiotic and free-living cyanobacteria performed on the 16S rRNA gene+ITS region is available with the online version of this paper.