skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Phosphorylation of the Bacillus subtilis Replication Controller YabA Plays a Role in Regulation of Sporulation and Biofilm Formation

Abstract

Bacillus subtilis cells can adopt different life-styles in response to various environmental cues, including planktonic cells during vegetative growth, sessile cells during biofilm formation and sporulation. While switching life-styles, bacteria must coordinate the progression of their cell cycle with their physiological status. Our current understanding of the regulatory pathways controlling the decision-making processes and triggering developmental switches highlights a key role of protein phosphorylation. The regulatory mechanisms that integrate the bacterial chromosome replication status with sporulation involve checkpoint proteins that target the replication initiator DnaA or the kinase phosphorelay controlling the master regulator Spo0A. B. subtilis YabA is known to interact with DnaA to prevent over-initiation of replication during vegetative growth. Here, we report that YabA is phosphorylated by YabT, a Ser/Thr kinase expressed during sporulation and biofilm formation. The phosphorylation of YabA has no effect on replication initiation control but hyper-phosphorylation of YabA leads to an increase in sporulation efficiency and a strong inhibition of biofilm formation. We also provide evidence that YabA phosphorylation affects the level of Spo0A-P in cells. In conclusion, these results indicate that YabA is a multifunctional protein with a dual role in regulating replication initiation and life-style switching, thereby providing a potential mechanism formore » cross-talk and coordination of cellular processes during adaptation to environmental change.« less

Authors:
; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
European Commission - Community Research and Development Information Service (CORDIS) - Seventh Framework Programme (FP7); USDOE Office of Science (SC)
OSTI Identifier:
1427555
Alternate Identifier(s):
OSTI ID: 1460839
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Published Article
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Name: Frontiers in Microbiology Journal Volume: 9; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Media SA
Country of Publication:
Switzerland
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Bacillus subtilis; Ser/Thr kinase; biofilm; replication initiation control; sporulation

Citation Formats

García García, Tránsito, Ventroux, Magali, Derouiche, Abderahmane, Bidnenko, Vladimir, Correia Santos, Sara, Henry, Céline, Mijakovic, Ivan, Noirot-Gros, Marie-Françoise, and Poncet, Sandrine. Phosphorylation of the Bacillus subtilis Replication Controller YabA Plays a Role in Regulation of Sporulation and Biofilm Formation. Switzerland: N. p., 2018. Web. doi:10.3389/fmicb.2018.00486.
García García, Tránsito, Ventroux, Magali, Derouiche, Abderahmane, Bidnenko, Vladimir, Correia Santos, Sara, Henry, Céline, Mijakovic, Ivan, Noirot-Gros, Marie-Françoise, & Poncet, Sandrine. Phosphorylation of the Bacillus subtilis Replication Controller YabA Plays a Role in Regulation of Sporulation and Biofilm Formation. Switzerland. doi:10.3389/fmicb.2018.00486.
García García, Tránsito, Ventroux, Magali, Derouiche, Abderahmane, Bidnenko, Vladimir, Correia Santos, Sara, Henry, Céline, Mijakovic, Ivan, Noirot-Gros, Marie-Françoise, and Poncet, Sandrine. Wed . "Phosphorylation of the Bacillus subtilis Replication Controller YabA Plays a Role in Regulation of Sporulation and Biofilm Formation". Switzerland. doi:10.3389/fmicb.2018.00486.
@article{osti_1427555,
title = {Phosphorylation of the Bacillus subtilis Replication Controller YabA Plays a Role in Regulation of Sporulation and Biofilm Formation},
author = {García García, Tránsito and Ventroux, Magali and Derouiche, Abderahmane and Bidnenko, Vladimir and Correia Santos, Sara and Henry, Céline and Mijakovic, Ivan and Noirot-Gros, Marie-Françoise and Poncet, Sandrine},
abstractNote = {Bacillus subtilis cells can adopt different life-styles in response to various environmental cues, including planktonic cells during vegetative growth, sessile cells during biofilm formation and sporulation. While switching life-styles, bacteria must coordinate the progression of their cell cycle with their physiological status. Our current understanding of the regulatory pathways controlling the decision-making processes and triggering developmental switches highlights a key role of protein phosphorylation. The regulatory mechanisms that integrate the bacterial chromosome replication status with sporulation involve checkpoint proteins that target the replication initiator DnaA or the kinase phosphorelay controlling the master regulator Spo0A. B. subtilis YabA is known to interact with DnaA to prevent over-initiation of replication during vegetative growth. Here, we report that YabA is phosphorylated by YabT, a Ser/Thr kinase expressed during sporulation and biofilm formation. The phosphorylation of YabA has no effect on replication initiation control but hyper-phosphorylation of YabA leads to an increase in sporulation efficiency and a strong inhibition of biofilm formation. We also provide evidence that YabA phosphorylation affects the level of Spo0A-P in cells. In conclusion, these results indicate that YabA is a multifunctional protein with a dual role in regulating replication initiation and life-style switching, thereby providing a potential mechanism for cross-talk and coordination of cellular processes during adaptation to environmental change.},
doi = {10.3389/fmicb.2018.00486},
journal = {Frontiers in Microbiology},
number = ,
volume = 9,
place = {Switzerland},
year = {2018},
month = {3}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.3389/fmicb.2018.00486

Citation Metrics:
Cited by: 2 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

A mechanism for cell cycle regulation of sporulation initiation in Bacillus subtilis
journal, August 2009

  • Veening, J. -W.; Murray, H.; Errington, J.
  • Genes & Development, Vol. 23, Issue 16
  • DOI: 10.1101/gad.528209

Molecular insights into the initiation of sporulation in Gram-positive bacteria: new technologies for an old phenomenon
journal, April 2005


Regulation of the replication cycle: conserved and diverse regulatory systems for DnaA and oriC
journal, March 2010

  • Katayama, Tsutomu; Ozaki, Shogo; Keyamura, Kenji
  • Nature Reviews Microbiology, Vol. 8, Issue 3
  • DOI: 10.1038/nrmicro2314

Condition-Dependent Transcriptome Reveals High-Level Regulatory Architecture in Bacillus subtilis
journal, March 2012


The Expanding Landscape of Moonlighting Proteins in Yeasts
journal, July 2016

  • Gancedo, Carlos; Flores, Carmen-Lisset; Gancedo, Juana M.
  • Microbiology and Molecular Biology Reviews, Vol. 80, Issue 3
  • DOI: 10.1128/MMBR.00012-16

Commitment to sporulation in Bacillus subtilis and its relationship to development of actinomycin resistance
journal, June 1969

  • Sterlini, Janet M.; Mandelstam, J.
  • Biochemical Journal, Vol. 113, Issue 1
  • DOI: 10.1042/bj1130029

Serine/Threonine Protein Kinases from Bacteria, Archaea and Eukarya Share a Common Evolutionary Origin Deeply Rooted in the Tree of Life
journal, January 2018

  • Stancik, Ivan Andreas; Šestak, Martin Sebastijan; Ji, Boyang
  • Journal of Molecular Biology, Vol. 430, Issue 1
  • DOI: 10.1016/j.jmb.2017.11.004

Compartmentalization of Gene Expression during Bacillus subtilis Spore Formation
journal, June 2004


Modeling cell-death patterning during biofilm formation
journal, November 2013


Sporulation of Bacillus subtilis
journal, December 2004


Functional dissection of YabA, a negative regulator of DNA replication initiation in Bacillus subtilis
journal, February 2006

  • Noirot-Gros, Marie-Françoise; Velten, M.; Yoshimura, M.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 7
  • DOI: 10.1073/pnas.0506914103

Regulation of the initiation of chromosomal replication in bacteria
journal, July 2007


Sticking together: building a biofilm the Bacillus subtilis way
journal, January 2013

  • Vlamakis, Hera; Chai, Yunrong; Beauregard, Pascale
  • Nature Reviews Microbiology, Vol. 11, Issue 3
  • DOI: 10.1038/nrmicro2960

Bistability and biofilm formation in Bacillus subtilis: Bistability and biofilm formation in Bacillus subtilis
journal, November 2007


Tetramerization and interdomain flexibility of the replication initiation controller YabA enables simultaneous binding to multiple partners
journal, November 2015

  • Felicori, Liza; Jameson, Katie H.; Roblin, Pierre
  • Nucleic Acids Research, Vol. 44, Issue 1
  • DOI: 10.1093/nar/gkv1318

The Sporulation Protein SirA Inhibits the Binding of DnaA to the Origin of Replication by Contacting a Patch of Clustered Amino Acids
journal, January 2011

  • Rahn-Lee, L.; Merrikh, H.; Grossman, A. D.
  • Journal of Bacteriology, Vol. 193, Issue 6
  • DOI: 10.1128/JB.01390-10

Localized cell death focuses mechanical forces during 3D patterning in a biofilm
journal, September 2012

  • Asally, M.; Kittisopikul, M.; Rue, P.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 46
  • DOI: 10.1073/pnas.1212429109

The Structural Basis for Control of Eukaryotic Protein Kinases
journal, July 2012


Fruiting body formation by Bacillus subtilis
journal, September 2001

  • Branda, S. S.; Gonzalez-Pastor, J. E.; Ben-Yehuda, S.
  • Proceedings of the National Academy of Sciences, Vol. 98, Issue 20
  • DOI: 10.1073/pnas.191384198

Regulating DNA Replication in Bacteria
journal, March 2013


Multiple Regulatory Systems Coordinate DNA Replication with Cell Growth in Bacillus subtilis
journal, October 2014


In Vitro Whole Genome DNA Binding Analysis of the Bacterial Replication Initiator and Transcription Factor DnaA
journal, May 2015


A major protein component of the Bacillus subtilis biofilm matrix
journal, February 2006


Bacterial single-stranded DNA-binding proteins are phosphorylated on tyrosine
journal, March 2006


Protein Flexibility Facilitates Quaternary Structure Assembly and Evolution
journal, May 2014


Control of Initiation of DNA Replication in Bacillus subtilis and Escherichia coli
journal, January 2017


Structure and interactions of the B acillus subtilis sporulation inhibitor of DNA replication, SirA, with domain I of DnaA : Structure of SirA-DnaA complex
journal, August 2014

  • Jameson, Katie H.; Rostami, Nadia; Fogg, Mark J.
  • Molecular Microbiology, Vol. 93, Issue 5
  • DOI: 10.1111/mmi.12713

Termination factor Rho: From the control of pervasive transcription to cell fate determination in Bacillus subtilis
journal, July 2017


Bacillus subtilis Two-Component System Sensory Kinase DegS Is Regulated by Serine Phosphorylation in Its Input Domain
journal, February 2011


A novel regulatory protein governing biofilm formation in Bacillus subtilis
journal, June 2008


Cell-Cycle-Dependent Spatial Sequestration of the DnaA Replication Initiator Protein in Bacillus subtilis
journal, December 2008

  • Soufo, Clarisse Defeu; Soufo, Hervé Joël Defeu; Noirot-Gros, Marie-Françoise
  • Developmental Cell, Vol. 15, Issue 6
  • DOI: 10.1016/j.devcel.2008.09.010

MoonProt: a database for proteins that are known to moonlight
journal, October 2014

  • Mani, Mathew; Chen, Chang; Amblee, Vaishak
  • Nucleic Acids Research, Vol. 43, Issue D1
  • DOI: 10.1093/nar/gku954

Bacillus subtilis YabA is involved in determining the timing and synchrony of replication initiation
journal, June 2005


Amyloid fibers provide structural integrity to Bacillus subtilis biofilms
journal, January 2010

  • Romero, D.; Aguilar, C.; Losick, R.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 5
  • DOI: 10.1073/pnas.0910560107

Replication Initiation Proteins Regulate a Developmental Checkpoint in Bacillus subtilis
journal, January 2001


SinR is a mutational target for fine-tuning biofilm formation in laboratory-evolved strains of Bacillus subtilis
journal, November 2014


Protein synthesis during cellular quiescence is inhibited by phosphorylation of a translational elongation factor
journal, June 2015

  • Pereira, Sandro F. F.; Gonzalez, Ruben L.; Dworkin, Jonathan
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 25
  • DOI: 10.1073/pnas.1505297112

Catabolic repression of bacterial sporulation.
journal, September 1965

  • Schaeffer, P.; Millet, J.; Aubert, J. P.
  • Proceedings of the National Academy of Sciences, Vol. 54, Issue 3
  • DOI: 10.1073/pnas.54.3.704

The functional analysis of YabA, which interacts with DnaA and regulates initiation of chromosome replication in Bacillus subtils
journal, January 2008

  • Cho, Eunha; Ogasawara, Naotake; Ishikawa, Shu
  • Genes & Genetic Systems, Vol. 83, Issue 2
  • DOI: 10.1266/ggs.83.111

The protein kinase family: conserved features and deduced phylogeny of the catalytic domains
journal, July 1988


Control of the replication initiator DnaA by an anti-cooperativity factor: Control of DnaA by an anti-cooperativity factor
journal, September 2011


Phosphorylation and functional analysis of the sporulation initiation factor Spo0A from Clostridium botulinum
journal, February 2006


Protein-tyrosine phosphorylation interaction network in Bacillus subtilis reveals new substrates, kinase activators and kinase cross-talk
journal, October 2014


The Primosomal Protein DnaD Inhibits Cooperative DNA Binding by the Replication Initiator DnaA in Bacillus subtilis
journal, July 2012

  • Bonilla, Carla Y.; Grossman, Alan D.
  • Journal of Bacteriology, Vol. 194, Issue 18
  • DOI: 10.1128/JB.00958-12

The Meiotic Checkpoint Network: Step-by-Step through Meiotic Prophase
journal, October 2014


Moonlighting proteins: An intriguing mode of multitasking
journal, April 2010

  • Huberts, Daphne H. E. W.; van der Klei, Ida J.
  • Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1803, Issue 4
  • DOI: 10.1016/j.bbamcr.2010.01.022

A master regulator for biofilm formation by Bacillus subtilis: Master regulator for biofilm formation
journal, December 2004


The DnaA inhibitor SirA acts in the same pathway as Soj (ParA) to facilitate oriC segregation during Bacillus subtilis sporulation
journal, August 2016

  • Duan, Yi; Huey, Jack D.; Herman, Jennifer K.
  • Molecular Microbiology, Vol. 102, Issue 3
  • DOI: 10.1111/mmi.13477

Genetic networks controlled by the bacterial replication initiator and transcription factor DnaA in Bacillus subtilis : Genes controlled by DnaA
journal, August 2017

  • Washington, Tracy A.; Smith, Janet L.; Grossman, Alan D.
  • Molecular Microbiology, Vol. 106, Issue 1
  • DOI: 10.1111/mmi.13755

Bacillus subtilis serine/threonine protein kinase YabT is involved in spore development via phosphorylation of a bacterial recombinase
journal, May 2013

  • Bidnenko, Vladimir; Shi, Lei; Kobir, Ahasanul
  • Molecular Microbiology, Vol. 88, Issue 5
  • DOI: 10.1111/mmi.12233

The Spo0A regulon of Bacillus subtilis: The Spo0A regulon
journal, November 2003


An expanded view of bacterial DNA replication
journal, June 2002

  • Noirot-Gros, M. -F.; Dervyn, E.; Wu, L. J.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 12
  • DOI: 10.1073/pnas.122040799

Just-in-Time Control of Spo0A Synthesis in Bacillus subtilis by Multiple Regulatory Mechanisms
journal, September 2011

  • Chastanet, Arnaud; Losick, Richard
  • Journal of Bacteriology, Vol. 193, Issue 22
  • DOI: 10.1128/JB.06057-11

Role of Protein Phosphorylation in the Regulation of Cell Cycle and DNA-Related Processes in Bacteria
journal, February 2016

  • Garcia-Garcia, Transito; Poncet, Sandrine; Derouiche, Abderahmane
  • Frontiers in Microbiology, Vol. 7
  • DOI: 10.3389/fmicb.2016.00184

Control of sporulation initiation in Bacillus subtilis
journal, December 2000