Cyclic AMP interferes with pattern formation in the cyanobacterium Anabaena variabilis

Smith, Gerald L.

doi:10.1016/0378-1097(81)90103-8

Cited by 9 publications

(8 citation statements)

References 15 publications

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“…In this case there was no addition of unusual compounds or mutations in genes that may have had pleiotropic effects. It is difficult to reconcile the results presented here as well as results of many previous studies that have shown that spaced heterocysts can form in the absence of nitrogen fixation (6,8,33,38,47) with a model that requires a gradient of any metabolite of nitrogen fixation. Further, while it has generally been accepted that starvation for fixed nitrogen in a cell is the major trigger for heterocyst differentiation, it is unlikely that cells producing sufficient fixed nitrogen for growth, using the Nif2 system under anoxic conditions, would be nitrogen starved.…”

Section: Discussioncontrasting

confidence: 49%

“…Overexpression of hetR leads to the formation of heterocysts in the presence of nitrate (6), as does a patS mutant (47). Methionine sulfoximine and 7-azatryptophan, as well as other amino acid analogues, allow heterocyst formation in the presence of fixed nitrogen (8,33). Glutamine synthetase mutants of A. variabilis have heterocysts and high levels of nitrogenase in the presence of ammonium, and they excrete ammonium into the medium (34).…”

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

Thiel

Pratte

2001

J Bacteriol

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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.

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confidence: 49%

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

Thiel

Pratte

2001

J Bacteriol

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“…In eukaryotes, cAMP regulates enzyme activity (11), channel activity (42), and gene expression (34) via the cAMP-dependent protein kinase. In cyanobacteria, it has been reported that cellular cAMP content is affected by growth conditions (17,22), that cAMP concentration changes rapidly in response to light-off and light-on signals (37) or to a pH shift (36), and that cAMP interferes with the pattern formation of heterocysts (43). However, it is still unknown whether cAMP functions as an intracellular signal molecule in cyanobacteria.…”

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Isolation and characterization of multiple adenylate cyclase genes from the cyanobacterium Anabaena sp. strain PCC 7120

Katayama

Ohmori

1997

J Bacteriol

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Adenylate cyclase genes, designated cyaA, cyaB1, cyaB2, cyaC, and cyaD, were isolated from the filamentous cyanobacterium Anabaena sp. strain PCC 7120 by complementation of a strain of Escherichia coli defective for the presence of cya. These genes encoded polypeptides consisting of 735, 859, 860, 1,155, and 546 amino acid residues, respectively. Deduced amino acid sequences of the regions near the C-terminal ends of these cya genes were similar to those of catalytic domains of eukaryotic adenylate cyclases. The remaining part of each cya gene towards its N-terminal end showed a characteristic structure. CyaA had two putative membrane-spanning regions. Both CyaB1 and CyaB2 had regions that were very similar to the cyclic GMP (cGMP)-binding domain of cGMP-stimulated cGMP phosphodiesterase. CyaC consisted of four distinct domains forming sequentially from the N terminus: a response regulator-like domain, a histidine kinase-like domain, a response regulatorlike domain, and the catalytic domain of adenylate cyclase. CyaD contained the forkhead-associated domain in its N-terminal region. Expression of these genes was examined by reverse transcription-PCR. The transcript of cyaC was shown to be predominant in this cyanobacterium. The cellular cyclic AMP level in the disruptant of the cyaC mutant was much lower than that in the wild type.Cyclic AMP (cAMP) regulates various biological activities in both prokaryotes and eukaryotes. In prokaryotes, cAMP and cAMP receptor protein regulate gene expression (7). In eukaryotes, cAMP regulates enzyme activity (11), channel activity (42), and gene expression (34) via the cAMP-dependent protein kinase. In cyanobacteria, it has been reported that cellular cAMP content is affected by growth conditions (17,22), that cAMP concentration changes rapidly in response to light-off and light-on signals (37) or to a pH shift (36), and that cAMP interferes with the pattern formation of heterocysts (43). However, it is still unknown whether cAMP functions as an intracellular signal molecule in cyanobacteria.Recently, we isolated adenylate cyclase (cya) genes from the filamentous cyanobacteria Anabaena cylindrica (26) and Spirulina platensis (52). Regions near the C-terminal ends of the adenylate cyclases of both cyanobacteria showed significant structural similarity to the catalytic domain of the adenylate cyclase of eukaryotes but showed no homology to that of prokaryotes such as Escherichia coli. Furthermore, cyanobacterial adenylate cyclases appeared to be membrane oriented.To study the physiological functions of these adenylate cyclases, disruption or overexpression of cya genes is indispensable. Unfortunately, both A. cylindrica and S. platensis are not transformable, so they are not suitable for this purpose. In this study, we isolated cya genes from a transformable cyanobacterium, Anabaena sp. strain PCC 7120, and constructed mutants defective in cya genes. Some physiological properties of these mutants were determined. MATERIALS AND METHODSStrains and growth conditions. Anabaena sp. s...

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“…Exceptionally high light intensity (4) and several chemicals often produce strings of two or more heterocysts where single heterocysts would otherwise be expected. Among the chemicals that produce strings of heterocysts are 7-azatryptophan (1,38,126), cyclic AMP (172), and rifampin (215), an inhibitor of RNA polymerase. Whether the strings produced chemically occur at random, suggestive of random initiation, or in a pattern, suggestive of a separate pattern-generating mechanism, has to our knowledge never been addressed.…”

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

Meeks

Elhai

2002

Microbiol Mol Biol Rev

365

361

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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

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Cyclic AMP interferes with pattern formation in the cyanobacterium Anabaena variabilis

Cited by 9 publications

References 15 publications

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

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

Isolation and characterization of multiple adenylate cyclase genes from the cyanobacterium Anabaena sp. strain PCC 7120

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

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