Cellular responses in the cyanobacterial symbiont during its vertical transfer between plant generations in the Azolla microphylla symbiosis

Summary•  The nitrogen‐fixing symbiosis between cyanobacteria and the water fern Azolla microphylla is, in contrast to other cyanobacteria–plant symbioses, the only one of a perpetual nature. The cyanobacterium is vertically transmitted between the plant generations, via vegetative fragmentation of the host or sexually within megasporocarps. In the latter process, subsets of the cyanobacterial population living endophytically in the Azolla leaves function as inocula for the new plant generations. •  Using electron microscopy and immunogold‐labeling, the fate of the cyanobacterium during colonization and development of the megasporocarp was revealed. •  On entering the indusium chamber of the megasporocarps as small‐celled motile cyanobacterial filaments (hormogonia), these differentiated into large thick‐walled akinetes (spores) in a synchronized manner. This process was accompanied by cytoplasmic reorganizations and the release of numerous membrane vesicles, most of which contained DNA, and the formation of a highly structured biofilm. •  Taken together the data revealed complex adaptations in the cyanobacterium during its transition between plant generations.