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 »
- Authors:
- Publication Date:
- Research Org.:
- Argonne National Laboratory (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. https://doi.org/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. https://doi.org/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 = {Wed Mar 21 00:00:00 EDT 2018},
month = {Wed Mar 21 00:00:00 EDT 2018}
}
https://doi.org/10.3389/fmicb.2018.00486
Web of Science
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
Molecular insights into the initiation of sporulation in Gram-positive bacteria: new technologies for an old phenomenon
journal, April 2005
- Stephenson, Keith; Lewis, Richard J.
- FEMS Microbiology Reviews, Vol. 29, Issue 2
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
Condition-Dependent Transcriptome Reveals High-Level Regulatory Architecture in Bacillus subtilis
journal, March 2012
- Nicolas, P.; Mader, U.; Dervyn, E.
- Science, Vol. 335, Issue 6072
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
The Pseudomonas fluorescens SBW25 wrinkly spreader biofilm requires attachment factor, cellulose fibre and LPS interactions to maintain strength and integrity
journal, September 2005
- Spiers, A. J.
- Microbiology, Vol. 151, Issue 9
Genetic and biochemical interactions between the bacterial replication initiator DnaA and the nucleoid-associated protein Rok in Bacillus subtilis : Interactions between DnaA and Rok in
journal, January 2017
- Seid, Charlotte A.; Smith, Janet L.; Grossman, Alan D.
- Molecular Microbiology, Vol. 103, Issue 5
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
Changes in DnaA-Dependent Gene Expression Contribute to the Transcriptional and Developmental Response of Bacillus subtilis to Manganese Limitation in Luria-Bertani Medium
journal, May 2010
- Hoover, S. E.; Xu, W.; Xiao, W.
- Journal of Bacteriology, Vol. 192, Issue 15
Modeling cell-death patterning during biofilm formation
journal, November 2013
- Ghosh, Pushpita; Ben-Jacob, Eshel; Levine, Herbert
- Physical Biology, Vol. 10, Issue 6
Sporulation of Bacillus subtilis
journal, December 2004
- Piggot, Patrick J.; Hilbert, David W.
- Current Opinion in Microbiology, Vol. 7, Issue 6
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
Regulation of the initiation of chromosomal replication in bacteria
journal, July 2007
- Zakrzewska-Czerwińska, Jolanta; Jakimowicz, Dagmara; Zawilak-Pawlik, Anna
- FEMS Microbiology Reviews, Vol. 31, Issue 4
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
Bistability and biofilm formation in Bacillus subtilis: Bistability and biofilm formation in Bacillus subtilis
journal, November 2007
- Chai, Yunrong; Chu, Frances; Kolter, Roberto
- Molecular Microbiology, Vol. 67, Issue 2
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
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
The Structural Basis for Control of Eukaryotic Protein Kinases
journal, July 2012
- Endicott, Jane A.; Noble, Martin E. M.; Johnson, Louise N.
- Annual Review of Biochemistry, Vol. 81, Issue 1
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
Regulating DNA Replication in Bacteria
journal, March 2013
- Skarstad, K.; Katayama, T.
- Cold Spring Harbor Perspectives in Biology, Vol. 5, Issue 4
Multiple Regulatory Systems Coordinate DNA Replication with Cell Growth in Bacillus subtilis
journal, October 2014
- Murray, Heath; Koh, Alan
- PLoS Genetics, Vol. 10, Issue 10
Evidence that entry into sporulation in Bacillus subtilis is governed by a gradual increase in the level and activity of the master regulator Spo0A
journal, September 2005
- Fujita, M.
- Genes & Development, Vol. 19, Issue 18
In Vitro Whole Genome DNA Binding Analysis of the Bacterial Replication Initiator and Transcription Factor DnaA
journal, May 2015
- Smith, Janet L.; Grossman, Alan D.
- PLOS Genetics, Vol. 11, Issue 5
A major protein component of the Bacillus subtilis biofilm matrix
journal, February 2006
- Branda, Steven S.; Chu, Frances; Kearns, Daniel B.
- Molecular Microbiology, Vol. 59, Issue 4
Bacterial single-stranded DNA-binding proteins are phosphorylated on tyrosine
journal, March 2006
- Mijakovic, I.
- Nucleic Acids Research, Vol. 34, Issue 5
Protein Flexibility Facilitates Quaternary Structure Assembly and Evolution
journal, May 2014
- Marsh, Joseph A.; Teichmann, Sarah A.
- PLoS Biology, Vol. 12, Issue 5
Control of Initiation of DNA Replication in Bacillus subtilis and Escherichia coli
journal, January 2017
- Jameson, Katie; Wilkinson, Anthony
- Genes, Vol. 8, Issue 1
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
Termination factor Rho: From the control of pervasive transcription to cell fate determination in Bacillus subtilis
journal, July 2017
- Bidnenko, Vladimir; Nicolas, Pierre; Grylak-Mielnicka, Aleksandra
- PLOS Genetics, Vol. 13, Issue 7
Bacillus subtilis Two-Component System Sensory Kinase DegS Is Regulated by Serine Phosphorylation in Its Input Domain
journal, February 2011
- Jers, Carsten; Kobir, Ahasanul; Søndergaard, Elsebeth Oline
- PLoS ONE, Vol. 6, Issue 2
A novel regulatory protein governing biofilm formation in Bacillus subtilis
journal, June 2008
- Chu, Frances; Kearns, Daniel B.; McLoon, Anna
- Molecular Microbiology, Vol. 68, Issue 5
Triggering sporulation in Bacillus subtilis with artificial two-component systems reveals the importance of proper Spo0A activation dynamics : Probing the role of Spo0A dynamics in sporulation
journal, August 2013
- Vishnoi, Monika; Narula, Jatin; Devi, Seram Nganbiton
- Molecular Microbiology
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
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
Genome-wide analysis of temporally regulated and compartment-specific gene expression in sporulating cells of Bacillus subtilis
journal, February 2005
- Steil, L.
- Microbiology, Vol. 151, Issue 2
Dynamic Association of the Replication Initiator and Transcription Factor DnaA with the Bacillus subtilis Chromosome during Replication Stress
journal, November 2008
- Breier, A. M.; Grossman, A. D.
- Journal of Bacteriology, Vol. 191, Issue 2
Bacillus subtilis YabA is involved in determining the timing and synchrony of replication initiation
journal, June 2005
- Hayashi, Miho; Ogura, Yoshitoshi; Harry, Elizabeth J.
- FEMS Microbiology Letters, Vol. 247, Issue 1
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
SinR is a mutational target for fine-tuning biofilm formation in laboratory-evolved strains of Bacillus subtilis
journal, November 2014
- Leiman, Sara A.; Arboleda, Laura C.; Spina, Joseph S.
- BMC Microbiology, Vol. 14, Issue 1
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
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
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
The protein kinase family: conserved features and deduced phylogeny of the catalytic domains
journal, July 1988
- Hanks, S.; Quinn, A.; Hunter, T.
- Science, Vol. 241, Issue 4861
Control of the replication initiator DnaA by an anti-cooperativity factor: Control of DnaA by an anti-cooperativity factor
journal, September 2011
- Merrikh, Houra; Grossman, Alan D.
- Molecular Microbiology, Vol. 82, Issue 2
Phosphorylation and functional analysis of the sporulation initiation factor Spo0A from Clostridium botulinum
journal, February 2006
- Worner, Kristina; Szurmant, Hendrik; Chiang, Christina
- Molecular Microbiology, Vol. 59, Issue 3
Protein-tyrosine phosphorylation interaction network in Bacillus subtilis reveals new substrates, kinase activators and kinase cross-talk
journal, October 2014
- Shi, Lei; Pigeonneau, Nathalie; Ventroux, Magali
- Frontiers in Microbiology, Vol. 5
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
The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis: Biofilm development in Bacillus subtilis
journal, December 2001
- Hamon, Mélanie A.; Lazazzera, Beth A.
- Molecular Microbiology, Vol. 42, Issue 5
The Meiotic Checkpoint Network: Step-by-Step through Meiotic Prophase
journal, October 2014
- Subramanian, V. V.; Hochwagen, A.
- Cold Spring Harbor Perspectives in Biology, Vol. 6, Issue 10
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
A master regulator for biofilm formation by Bacillus subtilis: Master regulator for biofilm formation
journal, December 2004
- Kearns, Daniel B.; Chu, Frances; Branda, Steven S.
- Molecular Microbiology, Vol. 55, Issue 3
Protein species and moonlighting proteins: Very small changes in a protein's covalent structure can change its biochemical function
journal, February 2016
- Jeffery, Constance J.
- Journal of Proteomics, Vol. 134
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
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
Biofilm formation at the air-liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose: Biofilm formation by P. fluorescens SBW25
journal, August 2003
- Spiers, Andrew J.; Bohannon, John; Gehrig, Stefanie M.
- Molecular Microbiology, Vol. 50, Issue 1
YabA and DnaD inhibit helix assembly of the DNA replication initiation protein DnaA: Regulation of DnaA by YabA and DnaD
journal, August 2013
- Scholefield, Graham; Murray, Heath
- Molecular Microbiology
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
The Spo0A regulon of Bacillus subtilis: The Spo0A regulon
journal, November 2003
- Molle, Virginie; Fujita, Masaya; Jensen, Shane T.
- Molecular Microbiology, Vol. 50, Issue 5
Biofilm formation by Bacillus subtilis requires an endoribonuclease-containing multisubunit complex that controls mRNA levels for the matrix gene repressor SinR : Multiprotein complex controlling SinR levels
journal, October 2015
- DeLoughery, Aaron; Dengler, Vanina; Chai, Yunrong
- Molecular Microbiology, Vol. 99, Issue 2
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
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
Works referencing / citing this record:
Protein post-translational modifications in bacteria
journal, September 2019
- Macek, Boris; Forchhammer, Karl; Hardouin, Julie
- Nature Reviews Microbiology, Vol. 17, Issue 11
In-depth analysis of Bacillus subtilis proteome identifies new ORFs and traces the evolutionary history of modified proteins
journal, November 2018
- Ravikumar, Vaishnavi; Nalpas, Nicolas C.; Anselm, Viktoria
- Scientific Reports, Vol. 8, Issue 1