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

Abstract

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.

Genome Erosion in a Nitrogen-Fixing Vertically Transmitted Endosymbiotic Multicellular Cyanobacterium

“…The Azolla endosymbiosis displays some evolutionary intriguing features. First, the host is able to maintain a small proportion of the cyanobiont population as an ‘inoculum’ between plant generations [14], [15]. This is accomplished through a complex and unique process using the Azolla reproductive organ, the sporocarp (predecessors to plant seeds), as transfer vehicle (Figure 1E).…”

“…This process relies on the capacity of the cyanobiont to differentiate motile filamentous hormogonia, which are attracted to and enter the sporocarp through a narrow pore. On entering the sporocarp the hormogonia differentiate into a resting stage (spores/akinetes), in which they remain dormant (extracellularly) until the plant germinates [15]. Secondly, the cyanobacterial partner seems to have lost (at least part of) its autonomy as it can not grow outside the plant [15], [16].…”

A Genetic and Chemical Perspective on Symbiotic Recruitment of Cyanobacteria of the Genus Nostoc into the Host Plant Blasia pusilla L.

“…The symbiotically competent Nostoc isolates were found along the entire Nostoc lineage of cyanobacteria (Papaefthimiou et al, 2008a) and do not show any patterns suggesting host specialization. The only exception is water-fern Azolla-Nostoc symbiosis, where the association is obligate and species specific for both and the partners are inseparable through the entire life cycle of the host (Papaefthimiou et al, 2008b; Zheng et al, 2009). The liverworts, hornworts and Gunnera produce the symbiotic structure before infection, and motile Nostoc filaments, hormogonia, enter these structures’ slime pores (Duckett et al, 1977; Rodgers and Stewart, 1977).…”

Cyanobacteria in Terrestrial Symbiotic Systems

“…During colonization of the megasporocarp, cyanobiont hormogonia enter through pores at the top of the indusium and then differentiate into akinetes in a synchronized manner. The details of this process are described in Zheng et al (2009). Papaefthimiou et al (2008b) and Sood et al (2008) studied cyanobacterial diversity in Azolla and found different cyanobacterial genotypes from different species and also diversity within a single Azolla species.…”