Multiple orphan histidine kinases interact directly with Spo0A to control the initiation of endospore formation in Clostridium acetobutylicum

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Multiple orphan histidine kinases interact directly with Spo0A to control the initiation of endospore formation in Clostridium acetobutylicum. / Heap, J. P.; Young, D. I.; Dago, A. E.; Minton, N. P.; Hoch, J. A.; Young, M.; Steiner, E.

In: Molecular Microbiology, Vol. 80, No. 3, 14.03.2011, p. 641-654.

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Heap, J. P. ; Young, D. I. ; Dago, A. E. ; Minton, N. P. ; Hoch, J. A. ; Young, M. ; Steiner, E. / Multiple orphan histidine kinases interact directly with Spo0A to control the initiation of endospore formation in Clostridium acetobutylicum. In: Molecular Microbiology. 2011 ; Vol. 80, No. 3. pp. 641-654.

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@article{af7c91c52abe43058b82f53a013d677f,
title = "Multiple orphan histidine kinases interact directly with Spo0A to control the initiation of endospore formation in Clostridium acetobutylicum",
abstract = "Summary The phosphorylated Spo0A transcription factor controls the initiation of endospore formation in Clostridium acetobutylicum, but genes encoding key phosphorelay components, Spo0F and Spo0B, are missing in the genome. We hypothesized that the five orphan histidine kinases of C. acetobutylicum interact directly with Spo0A to control its phosphorylation state. Sequential targeted gene disruption and gene expression profiling provided evidence for two pathways for Spo0A activation, one dependent on a histidine kinase encoded by cac0323, the other on both histidine kinases encoded by cac0903 and cac3319. Purified Cac0903 and Cac3319 kinases autophosphorylated and transferred phosphoryl groups to Spo0A in vitro, confirming their role in Spo0A activation in vivo. A cac0437 mutant hyper-sporulated, suggesting that Cac0437 is a modulator that prevents sporulation and maintains cellular Spo0A∼P homeostasis during growth. Accordingly, Cac0437 has apparently lost the ability to autophosphorylate in vitro; instead it catalyses the ATP-dependent dephosphorylation of Spo0A∼P releasing inorganic phosphate. Direct phosphorylation of Spo0A by histidine kinases and dephosphorylation by kinase-like proteins may be a common feature of the clostridia that may represent the ancestral state before the great oxygen event some 2.4 billion years ago, after which additional phosphorelay proteins were recruited in the evolutionary lineage that led to the bacilli.",
author = "Heap, {J. P.} and Young, {D. I.} and Dago, {A. E.} and Minton, {N. P.} and Hoch, {J. A.} and M. Young and E. Steiner",
note = "Steiner, E., Dago, A. E., Young, D. I., Heap, J. T., Minton, N. P., Hoch, J. A., Young, M.* (2011). Multiple orphan histidine kinases interact directly with Spo0A to control the initiation of endospore formation in Clostridium acetobutylicum Molecular Microbiology, 80, (3), 641-654, (A) IMPF: 05.01 ",
year = "2011",
month = mar,
day = "14",
doi = "10.1111/j.1365-2958.2011.07608.x",
language = "English",
volume = "80",
pages = "641--654",
journal = "Molecular Microbiology",
issn = "0950-382X",
publisher = "Wiley",
number = "3",

}

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TY - JOUR

T1 - Multiple orphan histidine kinases interact directly with Spo0A to control the initiation of endospore formation in Clostridium acetobutylicum

AU - Heap, J. P.

AU - Young, D. I.

AU - Dago, A. E.

AU - Minton, N. P.

AU - Hoch, J. A.

AU - Young, M.

AU - Steiner, E.

N1 - Steiner, E., Dago, A. E., Young, D. I., Heap, J. T., Minton, N. P., Hoch, J. A., Young, M.* (2011). Multiple orphan histidine kinases interact directly with Spo0A to control the initiation of endospore formation in Clostridium acetobutylicum Molecular Microbiology, 80, (3), 641-654, (A) IMPF: 05.01

PY - 2011/3/14

Y1 - 2011/3/14

N2 - Summary The phosphorylated Spo0A transcription factor controls the initiation of endospore formation in Clostridium acetobutylicum, but genes encoding key phosphorelay components, Spo0F and Spo0B, are missing in the genome. We hypothesized that the five orphan histidine kinases of C. acetobutylicum interact directly with Spo0A to control its phosphorylation state. Sequential targeted gene disruption and gene expression profiling provided evidence for two pathways for Spo0A activation, one dependent on a histidine kinase encoded by cac0323, the other on both histidine kinases encoded by cac0903 and cac3319. Purified Cac0903 and Cac3319 kinases autophosphorylated and transferred phosphoryl groups to Spo0A in vitro, confirming their role in Spo0A activation in vivo. A cac0437 mutant hyper-sporulated, suggesting that Cac0437 is a modulator that prevents sporulation and maintains cellular Spo0A∼P homeostasis during growth. Accordingly, Cac0437 has apparently lost the ability to autophosphorylate in vitro; instead it catalyses the ATP-dependent dephosphorylation of Spo0A∼P releasing inorganic phosphate. Direct phosphorylation of Spo0A by histidine kinases and dephosphorylation by kinase-like proteins may be a common feature of the clostridia that may represent the ancestral state before the great oxygen event some 2.4 billion years ago, after which additional phosphorelay proteins were recruited in the evolutionary lineage that led to the bacilli.

AB - Summary The phosphorylated Spo0A transcription factor controls the initiation of endospore formation in Clostridium acetobutylicum, but genes encoding key phosphorelay components, Spo0F and Spo0B, are missing in the genome. We hypothesized that the five orphan histidine kinases of C. acetobutylicum interact directly with Spo0A to control its phosphorylation state. Sequential targeted gene disruption and gene expression profiling provided evidence for two pathways for Spo0A activation, one dependent on a histidine kinase encoded by cac0323, the other on both histidine kinases encoded by cac0903 and cac3319. Purified Cac0903 and Cac3319 kinases autophosphorylated and transferred phosphoryl groups to Spo0A in vitro, confirming their role in Spo0A activation in vivo. A cac0437 mutant hyper-sporulated, suggesting that Cac0437 is a modulator that prevents sporulation and maintains cellular Spo0A∼P homeostasis during growth. Accordingly, Cac0437 has apparently lost the ability to autophosphorylate in vitro; instead it catalyses the ATP-dependent dephosphorylation of Spo0A∼P releasing inorganic phosphate. Direct phosphorylation of Spo0A by histidine kinases and dephosphorylation by kinase-like proteins may be a common feature of the clostridia that may represent the ancestral state before the great oxygen event some 2.4 billion years ago, after which additional phosphorelay proteins were recruited in the evolutionary lineage that led to the bacilli.

U2 - 10.1111/j.1365-2958.2011.07608.x

DO - 10.1111/j.1365-2958.2011.07608.x

M3 - Article

C2 - 21401736

VL - 80

SP - 641

EP - 654

JO - Molecular Microbiology

JF - Molecular Microbiology

SN - 0950-382X

IS - 3

ER -

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