Regulation of Cellular Differentiation in Filamentous Cyanobacteria in Free-Living and Plant-Associated Symbiotic Growth States

Abstract

Certain filamentous nitrogen-fixing cyanobacteria generate signals that direct their own multicellular development. They also respond to signals from plants that initiate or modulate differentiation, leading to the establishment of a symbiotic association. An objective of this review is to describe the mechanisms by which free-living cyanobacteria regulate their development and then to consider how plants may exploit cyanobacterial physiology to achieve stable symbioses. Cyanobacteria that are capable of forming plant symbioses can differentiate into motile filaments called hormogonia and into specialized nitrogen-fixing cells called heterocysts. Plant signals exert both positive and negative regulatory control on hormogonium differentiation. Heterocyst differentiation is a highly regulated process, resulting in a regularly spaced pattern of heterocysts in the filament. The evidence is most consistent with the pattern arising in two stages. First, nitrogen limitation triggers a nonrandomly spaced cluster of cells (perhaps at a critical stage of their cell cycle) to initiate differentiation. Interactions between an inhibitory peptide exported by the differentiating cells and an activator protein within them causes one cell within each cluster to fully differentiate, yielding a single mature heterocyst. In symbiosis with plants, heterocyst frequencies are increased 3- to 10-fold because, we propose, either differentation is initiated at an increased number of sites or resolution of differentiating clusters is incomplete. The physiology of symbiotically associated cyanobacteria raises the prospect that heterocyst differentiation proceeds independently of the nitrogen status of a cell and depends instead on signals produced by the plant partner

Carbon and nitrogen fixation and metabolite exchange in and between individual cells of Anabaena oscillarioides

“…These capabilities and the abundance of cyanobacteria in phytoplankton communities make these microorganisms keystone species in the global biogeochemical cycles of carbon and nitrogen. Under conditions of N limitation, some vegetative cells of Anabaena oscillarioides (a filamentous freshwater cyanobacterium) differentiate to form heterocysts non-growing, specialized cells in which N 2 is fixed into organic N (Stewart, 1973;Herrero et al, 1979;Kumar et al, 1983;Wolk, 1996Wolk, , 2000Meeks and Elhai, 2002). Because the enzyme that catalyzes N 2 fixation, nitrogenase, is inhibited by oxygen (Stewart, 1973;Gotto et al, 1979;Smith et al, 1987), heterocysts must be physically isolated from nearby vegetative cells, which are sites of oxygenic photosynthesis and CO 2 -fixation.…”

“…Finally, labeling of RNA and proteins with fluorescent probes, as well as immunolocalization experiments, has revealed the differential distribution and expression of various biomolecules (including nitrogenase and RuBisCO) in both heterocysts and vegetative cells (Murry et al, 1984). Hence, discrete processes occur within, and a rapid exchange of organic materials occurs between, heterocysts and vegetative cells (Wolk et al, 1976;Meeks and Elhai, 2002;Flores et al, 2006). However, much remains to be learned about the dynamics of CO 2 -and N 2 -fixation in filamentous cyanobacteria, particularly the synchronization, mobilization and exchange of C and N among cells (Flores et al, 2006).…”

NblA, a Key Protein of Phycobilisome Degradation, Interacts with ClpC, a HSP100 Chaperone Partner of a Cyanobacterial Clp Protease

“…In the filamentous, diazotrophic cyanobacteria Nostoc sp. PCC7120 (Nostoc 7120) and Anabaena variabilis ATCC 29413 this non-bleaching phenotype is most obvious in heterocysts, cells specialized for fixing N 2 under aerobic conditions, which usually contain only low levels of phycobiliproteins (18,19). Upon nitrogen stepdown, transcription of nblA is highly up-regulated (10, 15-17, 20 -22).…”

Current trends in high throughput proteomics in cyanobacteria

“…Likewise, global proteomics changes related to cellular differentiation have only been scarcely studied [58,59]. Other potential investigations, such as the proteomic changes in hormogonia, remain to be carried out [76]. For example, no accounts of substantive high throughput proteomics studies on circadian rhythm have been reported.…”