Cell fate regulation governed by a repurposed bacterial histidine kinase
Abstract
One of the simplest organisms to divide asymmetrically is the bacterium Caulobacter crescentus. The DivL pseudo-histidine kinase, positioned at one cell pole, regulates cell-fate by controlling the activation of the global transcription factor CtrA via an interaction with the response regulator (RR) DivK. DivL uniquely contains a tyrosine at the histidine phosphorylation site, and can achieve these regulatory functions in vivo without kinase activity. Determination of the DivL crystal structure and biochemical analysis of wild-type and site-specific DivL mutants revealed that the DivL PAS domains regulate binding specificity for DivK~P over DivK, which is modulated by an allosteric intramolecular interaction between adjacent domains. We discovered that DivL's catalytic domains have been repurposed as a phosphospecific RR input sensor, thereby reversing the flow of information observed in conventional histidine kinase (HK)-RR systems and coupling a complex network of signaling proteins for cell-fate regulation.
- Authors:
-
- Stanford Univ. School of Medicine, Stanford, CA (United States)
- SLAC National Accelerator Laboratory, Menlo Park, CA (United States)
- Rutgers Univ., New Brunswick, NJ (United States)
- Publication Date:
- Research Org.:
- SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1213908
- Grant/Contract Number:
- AC03-76SF00515
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS Biology (Online)
- Additional Journal Information:
- Journal Name: PLoS Biology (Online); Journal Volume: 12; Journal Issue: 10; Journal ID: ISSN 1545-7885
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; phosphorylation; xylose; binding analysis; cell cycle and cell division; point mutation; crystal structure; caulobacter; histidine
Citation Formats
Childers, W. Seth, Xu, Qingping, Mann, Thomas H., Mathews, Irimpan I., Blair, Jimmy A., Deacon, Ashley M., Shapiro, Lucy, and Stock, Ann M. Cell fate regulation governed by a repurposed bacterial histidine kinase. United States: N. p., 2014.
Web. doi:10.1371/journal.pbio.1001979.
Childers, W. Seth, Xu, Qingping, Mann, Thomas H., Mathews, Irimpan I., Blair, Jimmy A., Deacon, Ashley M., Shapiro, Lucy, & Stock, Ann M. Cell fate regulation governed by a repurposed bacterial histidine kinase. United States. https://doi.org/10.1371/journal.pbio.1001979
Childers, W. Seth, Xu, Qingping, Mann, Thomas H., Mathews, Irimpan I., Blair, Jimmy A., Deacon, Ashley M., Shapiro, Lucy, and Stock, Ann M. Tue .
"Cell fate regulation governed by a repurposed bacterial histidine kinase". United States. https://doi.org/10.1371/journal.pbio.1001979. https://www.osti.gov/servlets/purl/1213908.
@article{osti_1213908,
title = {Cell fate regulation governed by a repurposed bacterial histidine kinase},
author = {Childers, W. Seth and Xu, Qingping and Mann, Thomas H. and Mathews, Irimpan I. and Blair, Jimmy A. and Deacon, Ashley M. and Shapiro, Lucy and Stock, Ann M.},
abstractNote = {One of the simplest organisms to divide asymmetrically is the bacterium Caulobacter crescentus. The DivL pseudo-histidine kinase, positioned at one cell pole, regulates cell-fate by controlling the activation of the global transcription factor CtrA via an interaction with the response regulator (RR) DivK. DivL uniquely contains a tyrosine at the histidine phosphorylation site, and can achieve these regulatory functions in vivo without kinase activity. Determination of the DivL crystal structure and biochemical analysis of wild-type and site-specific DivL mutants revealed that the DivL PAS domains regulate binding specificity for DivK~P over DivK, which is modulated by an allosteric intramolecular interaction between adjacent domains. We discovered that DivL's catalytic domains have been repurposed as a phosphospecific RR input sensor, thereby reversing the flow of information observed in conventional histidine kinase (HK)-RR systems and coupling a complex network of signaling proteins for cell-fate regulation.},
doi = {10.1371/journal.pbio.1001979},
journal = {PLoS Biology (Online)},
number = 10,
volume = 12,
place = {United States},
year = {Tue Oct 28 00:00:00 EDT 2014},
month = {Tue Oct 28 00:00:00 EDT 2014}
}
Web of Science
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- Rodriguez-Beltran, Jeronimo; Hernandez-Beltran, J. Carlos R.; DelaFuente, Javier
- Nature Ecology & Evolution, Vol. 2, Issue 5
Reciprocal control of motility and biofilm formation by the PdhS2 two-component sensor kinase of Agrobacterium tumefaciens
journal, February 2019
- Heindl, Jason E.; Crosby, Daniel; Brar, Sukhdev
- Microbiology, Vol. 165, Issue 2
Cyclic di-GMP mediates a histidine kinase/phosphatase switch by noncovalent domain cross-linking
journal, September 2016
- Dubey, Badri N.; Lori, Christian; Ozaki, Shogo
- Science Advances, Vol. 2, Issue 9
Polar Organizing Protein PopZ Is Required for Chromosome Segregation in Agrobacterium tumefaciens
journal, September 2017
- Ehrle, Haley M.; Guidry, Jacob T.; Iacovetto, Rebecca
- Journal of Bacteriology, Vol. 199, Issue 17
Absolute Measurements of mRNA Translation in Caulobacter crescentus Reveal Important Fitness Costs of Vitamin B 12 Scavenging
journal, May 2019
- Aretakis, James R.; Gega, Alisa; Schrader, Jared M.
- mSystems, Vol. 4, Issue 4
Regulation of bacterial surface attachment by a network of sensory transduction proteins
journal, May 2019
- Reyes Ruiz, Leila M.; Fiebig, Aretha; Crosson, Sean
- PLOS Genetics, Vol. 15, Issue 5
Comparative Analysis ofWolbachiaGenomes Reveals Streamlining and Divergence of Minimalist Two-Component Systems
journal, May 2015
- Christensen, Steen; Serbus, Laura Renee
- G3 Genes|Genomes|Genetics, Vol. 5, Issue 5
Redefining bacterial origins of replication as centralized information processors
journal, June 2015
- Marczynski, Gregory T.; Rolain, Thomas; Taylor, James A.
- Frontiers in Microbiology, Vol. 6