DNA Complexed Structure of the Key Transcription Factor Initiating Development in Sporulating Bacteria

Zhao, Haiyan; Msadek, Tarek; Zapf, James; Madhusudan, M. D.; Hoch, James A.; Varughese, Kottayil I.

doi:10.1016/s0969-2126(02)00803-1

Cited by 62 publications

(92 citation statements)

References 38 publications

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“…In the DNA-binding domain all of the residues known to make contact with the DNA target of Spo0A, the 0A box, are identical, which suggests that the sequence of the 0A box is invariant in sporulating bacteria (39). Amino acid sequence conservation is also apparent in the Spo0F and Spo0B components of the phosphorelay (33).…”

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confidence: 99%

Characterization of Sporulation Histidine Kinases ofBacillus anthracis

et al. 2005

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The initiation of sporulation in Bacillus species is regulated by the phosphorelay signal transduction pathway, which is activated by several histidine sensor kinases in response to cellular and metabolic signals.Comparison of the protein components of the phosphorelay between Bacillus subtilis and Bacillus anthracis revealed high homology in the phosphorelay orthologs of Spo0F, Spo0B, and Spo0A. The sensor domains of sensor histidine kinases are poorly conserved between species, making ortholog recognition tenuous. Putative sporulation sensor histidine kinases of B. anthracis were identified by homology to the HisKA domain of B. subtilis sporulation sensor histidine kinases, which interacts with Spo0F. Nine possible kinases were uncovered, and their genes were assayed for complementation of kinase mutants of B. subtilis, for ability to drive lacZ expression in B. subtilis and B. anthracis, and for the effect of deletion of each on the sporulation of B. anthracis. Five of the nine sensor histidine kinases were inferred to be capable of inducing sporulation in B. anthracis. Four of the sensor kinases could not be shown to induce sporulation; however, the genes for two of these were frameshifted in all B. anthracis strains and one of these was also frameshifted in the pathogenic pXO1-bearing Bacillus cereus strain G9241. It is proposed that acquisition of plasmid pXO1 and pathogenicity may require a dampening of sporulation regulation by mutational selection of sporulation sensor histidine kinase defects. The sporulation of B. anthracis ex vivo appears to result from any one or a combination of the sporulation sensor histidine kinases remaining.

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Characterization of Sporulation Histidine Kinases ofBacillus anthracis

et al. 2005

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“…The target sites reveal a consensus binding sequence, TTTGTCRAA, which is known as the 0A box (23). The crystal structure of the C-terminal (DNA-binding) domain of the Bacillus stearothermophilus ortholog in a complex with 0A box sequences has been solved (32). This structure reveals contacts of the DNA-binding domain with bases in the 0A box and with the DNA backbone and has led to the suggestion that Spo0AϳP dimers are capable of forming tandem arrays in a head-to-tail arrangement along the DNA (32).…”

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confidence: 99%

“…The crystal structure of the C-terminal (DNA-binding) domain of the Bacillus stearothermophilus ortholog in a complex with 0A box sequences has been solved (32). This structure reveals contacts of the DNA-binding domain with bases in the 0A box and with the DNA backbone and has led to the suggestion that Spo0AϳP dimers are capable of forming tandem arrays in a head-to-tail arrangement along the DNA (32). It was suggested that such arrays may form in the regulatory region for genes such as spoIIA, spoIIE, and spoIIG that exhibit multiple 0A boxes in tandem extending far upstream from the start site of transcription.…”

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Just-in-Time Control of Spo0A Synthesis in Bacillus subtilis by Multiple Regulatory Mechanisms

Chastanet

Losick

2011

J Bacteriol

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The response regulator Spo0A governs multiple developmental processes in Bacillus subtilis, including most conspicuously sporulation. Spo0A is activated by phosphorylation via a multicomponent phosphorelay. Previous work has shown that the Spo0A protein is not rate limiting for sporulation. Rather, Spo0A is present at high levels in growing cells, rapidly rising to yet higher levels under sporulation-inducing conditions, suggesting that synthesis of the response regulator is subject to a just-in-time control mechanism. Transcription of spo0A is governed by a promoter switching mechanism, involving a vegetative, A -recognized promoter, P v , and a sporulation H -recognized promoter, P s , that is under phosphorylated Spo0A (Spo0AϳP) control. The spo0A regulatory region also contains four (including one identified in the present work) conserved elements that conform to the consensus binding site for Spo0AϳP binding sites. These are herein designated O 1 , O 2 , O 3 , and O 4 in reverse order of their proximity to the coding sequence. Here we report that O 1 is responsible for repressing P v during the transition to stationary phase, that O 2 is responsible for repressing P s during growth, that O 3 is responsible for activating P s at the start of sporulation, and that O 4 is dispensable for promoter switching. We also report that Spo0A synthesis is subject to a posttranscriptional control mechanism such that translation of mRNAs originating from P v is impeded due to RNA secondary structure whereas mRNAs originating from P s are fully competent for protein synthesis. We propose that the opposing actions of O 2 and O 3 and the enhanced translatability of mRNAs originating from P s create a highly sensitive, self-reinforcing switch that is responsible for producing a burst of Spo0A synthesis at the start of sporulation.

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“…Our nuclear magnetic resonance (NMR) structure of Spo0F with John Cavanagh defined the flexible regions found in conformers that we proposed to be the regions responsible for interaction with other proteins of the phosphorelay (12). Moreover, we captured the structure of Spo0A bound to its DNA target, in a crystal, allowing determination of residues important for binding (101).…”

Section: Understanding Molecular Recognition By Protein Structure Andmentioning

confidence: 99%

A Life inBacillus subtilisSignal Transduction

Hoch

2017

Annu. Rev. Microbiol.

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This is a tale of how technology drove the discovery of the molecular basis for signal transduction in the initiation of sporulation in Bacillus subtilis and in bacterial two-component systems. It progresses from genetics to cloning and sequencing to biochemistry to structural biology to an understanding of how proteins evolve interaction specificity and to identification of interaction surfaces by statistical physics. This is about how the people in my laboratory accomplished this feat; without them little would have been done.

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DNA Complexed Structure of the Key Transcription Factor Initiating Development in Sporulating Bacteria

Cited by 62 publications

References 38 publications

Characterization of Sporulation Histidine Kinases ofBacillus anthracis

Characterization of Sporulation Histidine Kinases ofBacillus anthracis

Just-in-Time Control of Spo0A Synthesis in Bacillus subtilis by Multiple Regulatory Mechanisms

A Life inBacillus subtilisSignal Transduction

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