Effect on Heterocyst Differentiation of Nitrogen Fixation in Vegetative Cells of the Cyanobacterium Anabaena variabilis ATCC 29413

Abstract

Heterocysts are terminally differentiated cells of some filamentous cyanobacteria that fix nitrogen for the entire filament under oxic growth conditions. Anabaena variabilis ATCC 29413 is unusual in that it has two Mo-dependent nitrogenases; one, called Nif1, functions in heterocysts, while the second, Nif2, functions under anoxic conditions in vegetative cells. Both nitrogenases depended on expression of the global regulatory protein NtcA. It has long been thought that a product of nitrogen fixation in heterocysts plays a role in maintenance of the spaced pattern of heterocyst differentiation. This model assumes that each cell in a filament senses its own environment in terms of nitrogen sufficiency and responds accordingly in terms of differentiation. Expression of the Nif2 nitrogenase under anoxic conditions in vegetative cells was sufficient to support long-term growth of a nif1 mutant; however, that expression did not prevent differentiation of heterocysts and expression of the nif1 nitrogenase in either the nif1 mutant or the wild-type strain. This suggested that the nitrogen sufficiency of individual cells in the filament did not affect the signal that induces heterocyst differentiation. Perhaps there is a global mechanism by which the filament senses nitrogen sufficiency or insufficiency based on the external availability of fixed nitrogen. The filament would then respond by producing heterocyst differentiation signals that affect the entire filament. This does not preclude cell-to-cell signaling in the maintenance of heterocyst pattern but suggests that overall control of the process is not controlled by nitrogen insufficiency of individual cells.

Hydrogenases and Hydrogen Metabolism of Cyanobacteria

“…In contrast to these results, a low level of hupL expression (detected by RT-PCR) has been found in A. variabilis ATCC 29413 vegetative cells grown with the addition of ammonia (28). Interest- ingly, when exposed to anaerobic conditions A. variabilis synthesizes a second Mo nitrogenase cellularly localized in the vegetative cells (199). The concomitant induction of the already identified uptake hydrogenase (79) or a possible alternative uptake hydrogenase deserves further studies.…”

“…Heterocyst formation does not take place randomly within the filament. Recently, it was proposed that this process in Anabaena variabilis is not controlled by individual cells but by the entire filament (199). The filament senses the nitrogen status and responds by producing heterocyst differentiation signals.…”

“…The filament senses the nitrogen status and responds by producing heterocyst differentiation signals. However, this does not exclude cell-to-cell signaling in the maintenance of heterocyst pattern (26,199,220), and it has been shown that the small diffusible peptide PatS and products of nitrogen fixation control heterocyst differentiation in Anabaena strain PCC 7120 (226,227). The heterocyst provides a microanaerobic environment suitable for the functioning of nitrogenase since (i) it lacks photosystem II activity, (ii) it has a higher rate of respiratory oxygen consumption, and (iii) it is surrounded by a thick envelope that limits the diffusion of oxygen through the cell wall (56,221).…”

“…The first one (the so-called conventional nitrogenase, encoded by the nif1 gene cluster) functions in heterocysts. The second enzyme (encoded by the nif2 gene cluster) functions strictly under anaerobic conditions in vegetative cells only (199).…”

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

“…This result implies that the suppressor signal must be a consequence of ammonium assimilation, such as increased glutamine or decreased ␣-ketoglutarate levels. This conclusion has been questioned as the result of experiments exploiting the ability of A. variabilis to express an alternative nitrogenase in vegetative cells under anoxic growth conditions (189). Under these conditions, this strain can grow on N 2 , even when the heterocyst-specific nitrogenase is inactivated by mutation.…”