Energy and calcium ion dependence of proteolysis during sporulation of Bacillus subtilis cells

Ohara, Masaru; Hageman, James H.

doi:10.1128/jb.172.8.4161-4170.1990

Cited by 41 publications

(21 citation statements)

References 46 publications

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“…In addition, protein degradation during sporulation of Bacillus subtilis has been reported to be a calcium-dependent process (O'Hara & Hageman, 1990), and in cyanobacteria it has long been recognized that there is a correlation between extracellular calcium concentration and heterocyst frequency (Smith & Wilkins, 1988;Zhao et al, 1991;Onek & Smith, 1992). However, our work represents probably the first example of continuous monitoring of [Ca 2+ ] i during a process of cell differentiation in a prokaryotic organism.…”

Section: Discussionmentioning

confidence: 71%

“…Therefore it is tempting to correlate the calcium transient with the signalling for proteolysis of phycobiliproteins. In fact, in B. subtilis a Ca 2+ influx has been shown to be essential for the early proteolysis that takes place during sporulation (O'Hara & Hageman, 1990;Shyu & Foegeding, 1991;Dominguez et al, 1999). However, the relevance of the calcium-dependent protease in the process of heterocyst differentiation remains unclear since Lockau et al (1988) and Maldener et al (1991) demonstrated that this protease is not essential for the development of functional heterocysts.…”

Section: Discussionmentioning

confidence: 99%

“…Since Ca 2+ was first studied in bacteria fifty years ago (Norris & Jensen, 1957) it has been implicated in a broad range of physiological processes in prokaryotes that include chemotaxis and motility (Tisa & Adler, 1992Watkins et al, 1995;Pitta et al, 1997), pathogenesis (Rose et al, 1993;Straley et al, 1993), the cell cycle and the control of the initiation of replication (Jiménez-Sanchez et al, 1993;Yu & Margolin, 1997), quorum sensing (Wherten & Lundgren, 2001) and spore and fruiting body formation (Inouye et al, 1983;O'Hara & Hageman, 1990). In many cases, the involvement of Ca 2+ in the regulation of cellular processes has been roughly described in terms of an influx or efflux of Ca 2+ from the cytosol.…”

Section: Introductionmentioning

confidence: 99%

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A calcium signal is involved in heterocyst differentiation in the cyanobacterium Anabaena sp. PCC7120

et al. 2004

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The impact of calcium signals in virtually all cells has led to the study of their role in prokaryotic organisms as stress response modulators. Cell differentiation in adverse conditions is a common Ca2+-requiring response. Nitrogen starvation induces the differentiation of N2-fixing heterocysts in the filamentous cyanobacterium Anabaena sp. PCC7120. This paper reports the use of a recombinant strain of this organism expressing the photoprotein aequorin to monitor the intracellular free-calcium concentration during the course of heterocyst differentiation. A specific calcium signature that is triggered exclusively when cells are deprived of combined nitrogen and generated by intracellular calcium stores was identified. The intracellular calcium signal was manipulated by treatment with specific calcium drugs, and the effect of such manipulation on the process of heterocyst differentiation was subsequently assessed. Suppression, magnification or poor regulation of this signal prevented the process of heterocyst differentiation, thereby suggesting that a calcium signal with a defined set of kinetic parameters may be required for differentiation. A hetR mutant of Anabaena sp. PCC7120 that cannot differentiate into heterocysts retains, however, the capacity to generate the calcium transient in response to nitrogen deprivation, strongly suggesting that Ca2+ may be involved in a very early step of the differentiation process.

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Section: Discussionmentioning

confidence: 71%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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A calcium signal is involved in heterocyst differentiation in the cyanobacterium Anabaena sp. PCC7120

et al. 2004

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“…Intracellular alanine is probably generated during sporulation through the turnover of proteins. It has long been known that bulk protein turnover increases during sporulation (30,47,51). In addition, turnover of specific proteins is known to increase during sporulation (25,28,38,45).…”

Section: Resultsmentioning

confidence: 99%

“…The tricarboxylic acid cycle seems to play a role in the generation of energy during sporulation, as mutants that are defective in tricarboxylic acid cycle enzymes are defective in sporulation (13,18,56). Protein turnover is known to increase during sporulation (30,47) and probably plays a role in generating substrates (peptides and amino acids) for further metabolism and new macromolecular syn-thesis.…”

mentioning

confidence: 99%

Alanine dehydrogenase (ald) is required for normal sporulation in Bacillus subtilis

1993

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The ski22::Tn917lac insertion mutation in Bacillus subtilis was isolated in a screen for mutations that cause a defect in sporulation but are suppressed by the presence or overexpression of the histidine protein kinase encoded by kinA (spoIIJ). The ski22::Tn9171ac insertion mutation was in ald, the gene encoding alanine dehydrogenase. Alanine dehydrogenase catalyzes the deamination of alanine to pyruvate and ammonia and is needed for growth when alanine is the sole carbon or nitrogen source. The sporulation defect caused by null mutations in ald was partly relieved by the addition of pyruvate at a high concentration, indicating that the normal role of alanine dehydrogenase in sporulation might be to generate pyruvate to provide an energy source for sporulation. The spoVN::Tn9l7 mutation was also found to be an allele of aid. Transcription of ald was induced very early during sporulation and by the addition of exogenous alanine during growth. Expression of ald was normal in all of the regulatory mutants tested, including spoOA, spoOH, spoOK, comA, sigB, and sigD mutants. The only gene in which mutations affected expression of ald was ald itself. This regulation is probably related to the metabolism of alanine.Cells of Bacillus subtilis can differentiate into dormant heat-resistant endospores under appropriate environmental conditions. Regulatory events during the initiation of sporulation lead to the formation of an asymmetric cell division septum, generating two distinct cell types. The smaller cell, or forespore, develops into the mature spore after being engulfed by the larger cell, the mother cell (reviewed in reference 10). Eventually, the mother cell lyses, releasing the mature heatresistant endospore.Dramatic changes in gene expression, physiology, and metabolism underlie the morphological changes associated with spore formation. A variety of regulatory circuits and genes required for sporulation have been characterized. In addition, many genes that are expressed during sporulation are not essential for development (10). While much work has focused on gene expression and regulation, relatively little is known about metabolism and the generation of energy for synthesis of new products required for the morphological development that occurs during sporulation. The tricarboxylic acid cycle seems to play a role in the generation of energy during sporulation, as mutants that are defective in tricarboxylic acid cycle enzymes are defective in sporulation (13,18,56). Protein turnover is known to increase during sporulation (30, 47) and probably plays a role in generating substrates (peptides and amino acids) for further metabolism and new macromolecular synthesis.Previously, we described the isolation and characterization of mutations that caused a defect in sporulation but could be partially suppressed by the presence or overproduction of the histidine protein kinase encoded by kinA (19,20,37). These mutations were called ski (pronounced "sky," for suppressed by kinase) and include spoOK (37) and bofA (20,36). Kin...

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Intracellular serine protease-4, a new intracellular serine protease activity from Bacillus subtilis

Sheehan

Switzer

1991

Arch. Microbiol.

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A previously undiscovered intracellular serine protease activity, which we have called intracellular serine protease-4, was identified in extracts of stationary Bacillus subtilis cells, purified 260 fold from the cytoplasmic fraction, and characterized. The new protease was stable and active in the absence of Ca2+ ions and hydrolyzed azocasein and the chromogenic substrate carbobenzoxy-carbonyl-alanyl-alanyl-leucyl-p-nitroanilide, but not azocollagen or a variety of other chromogenic substrates. The protease was strongly inhibited by phenylmethylsulfonylfluoride, chymostatin and antipain, but not by chelators, sulfhydryl-reactive agents or trypsin inhibitors. Its activity was stimulated by Ca2+ ions and gramicidin S; its pH and temperature optima were 9.0 and 37 degrees C, respectively. Although intracellular serine protease-4 was immunochemically distinct from intracellular serine protease-1, it was absent from a mutant in which the gene encoding the latter was disrupted.

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Energy and calcium ion dependence of proteolysis during sporulation of Bacillus subtilis cells

Cited by 41 publications

References 46 publications

A calcium signal is involved in heterocyst differentiation in the cyanobacterium Anabaena sp. PCC7120

A calcium signal is involved in heterocyst differentiation in the cyanobacterium Anabaena sp. PCC7120

Alanine dehydrogenase (ald) is required for normal sporulation in Bacillus subtilis

Intracellular serine protease-4, a new intracellular serine protease activity from Bacillus subtilis

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