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

García García, Tránsito; Ventroux, Magali; Derouiche, Abderahmane; Bidnenko, Vladimir; Correia Santos, Sara; Henry, Céline; Mijakovic, Ivan; Noirot-Gros, Marie-Françoise; Poncet, Sandrine

doi:10.3389/fmicb.2018.00486

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

Journal Article · Wed Mar 21 00:00:00 EDT 2018 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2018.00486· OSTI ID:1427555

García García, Tránsito; Ventroux, Magali; Derouiche, Abderahmane; Bidnenko, Vladimir; Correia Santos, Sara; Henry, Céline; Mijakovic, Ivan; Noirot-Gros, Marie-Françoise; Poncet, Sandrine

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.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: European Commission - Community Research and Development Information Service (CORDIS) - Seventh Framework Programme (FP7); USDOE Office of Science (SC)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1427555

Alternate ID(s):: OSTI ID: 1460839

Journal Information:: Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 9; ISSN 1664-302X

Publisher:: Frontiers Media SACopyright Statement

Country of Publication:: Switzerland

Language:: English

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Cited by: 10 works

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References (61)

A mechanism for cell cycle regulation of sporulation initiation in Bacillus subtilis Veening, J. -W.; Murray, H.; Errington, J. Genes & Development, Vol. 23, Issue 16 https://doi.org/10.1101/gad.528209	journal	August 2009
Molecular insights into the initiation of sporulation in Gram-positive bacteria: new technologies for an old phenomenon Stephenson, Keith; Lewis, Richard J. FEMS Microbiology Reviews, Vol. 29, Issue 2 https://doi.org/10.1016/j.fmrre.2004.10.003	journal	April 2005
Regulation of the replication cycle: conserved and diverse regulatory systems for DnaA and oriC Katayama, Tsutomu; Ozaki, Shogo; Keyamura, Kenji Nature Reviews Microbiology, Vol. 8, Issue 3 https://doi.org/10.1038/nrmicro2314	journal	March 2010
Condition-Dependent Transcriptome Reveals High-Level Regulatory Architecture in Bacillus subtilis Nicolas, P.; Mader, U.; Dervyn, E. Science, Vol. 335, Issue 6072 https://doi.org/10.1126/science.1206848	journal	March 2012
Commitment to sporulation in Bacillus subtilis and its relationship to development of actinomycin resistance Sterlini, Janet M.; Mandelstam, J. Biochemical Journal, Vol. 113, Issue 1 https://doi.org/10.1042/bj1130029	journal	June 1969
The Pseudomonas fluorescens SBW25 wrinkly spreader biofilm requires attachment factor, cellulose fibre and LPS interactions to maintain strength and integrity Spiers, A. J. Microbiology, Vol. 151, Issue 9 https://doi.org/10.1099/mic.0.27984-0	journal	September 2005
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 Seid, Charlotte A.; Smith, Janet L.; Grossman, Alan D. Molecular Microbiology, Vol. 103, Issue 5 https://doi.org/10.1111/mmi.13590	journal	January 2017
Serine/Threonine Protein Kinases from Bacteria, Archaea and Eukarya Share a Common Evolutionary Origin Deeply Rooted in the Tree of Life Stancik, Ivan Andreas; Šestak, Martin Sebastijan; Ji, Boyang Journal of Molecular Biology, Vol. 430, Issue 1 https://doi.org/10.1016/j.jmb.2017.11.004	journal	January 2018
Changes in DnaA-Dependent Gene Expression Contribute to the Transcriptional and Developmental Response of Bacillus subtilis to Manganese Limitation in Luria-Bertani Medium Hoover, S. E.; Xu, W.; Xiao, W. Journal of Bacteriology, Vol. 192, Issue 15 https://doi.org/10.1128/JB.00210-10	journal	May 2010
Modeling cell-death patterning during biofilm formation Ghosh, Pushpita; Ben-Jacob, Eshel; Levine, Herbert Physical Biology, Vol. 10, Issue 6 https://doi.org/10.1088/1478-3975/10/6/066006	journal	November 2013
Sporulation of Bacillus subtilis Piggot, Patrick J.; Hilbert, David W. Current Opinion in Microbiology, Vol. 7, Issue 6 https://doi.org/10.1016/j.mib.2004.10.001	journal	December 2004
Functional dissection of YabA, a negative regulator of DNA replication initiation in Bacillus subtilis Noirot-Gros, Marie-Françoise; Velten, M.; Yoshimura, M. Proceedings of the National Academy of Sciences, Vol. 103, Issue 7 https://doi.org/10.1073/pnas.0506914103	journal	February 2006
Regulation of the initiation of chromosomal replication in bacteria Zakrzewska-Czerwińska, Jolanta; Jakimowicz, Dagmara; Zawilak-Pawlik, Anna FEMS Microbiology Reviews, Vol. 31, Issue 4 https://doi.org/10.1111/j.1574-6976.2007.00070.x	journal	July 2007
Sticking together: building a biofilm the Bacillus subtilis way Vlamakis, Hera; Chai, Yunrong; Beauregard, Pascale Nature Reviews Microbiology, Vol. 11, Issue 3 https://doi.org/10.1038/nrmicro2960	journal	January 2013
Bistability and biofilm formation in Bacillus subtilis: Bistability and biofilm formation in Bacillus subtilis Chai, Yunrong; Chu, Frances; Kolter, Roberto Molecular Microbiology, Vol. 67, Issue 2 https://doi.org/10.1111/j.1365-2958.2007.06040.x	journal	November 2007
Tetramerization and interdomain flexibility of the replication initiation controller YabA enables simultaneous binding to multiple partners Felicori, Liza; Jameson, Katie H.; Roblin, Pierre Nucleic Acids Research, Vol. 44, Issue 1 https://doi.org/10.1093/nar/gkv1318	journal	November 2015
Localized cell death focuses mechanical forces during 3D patterning in a biofilm Asally, M.; Kittisopikul, M.; Rue, P. Proceedings of the National Academy of Sciences, Vol. 109, Issue 46 https://doi.org/10.1073/pnas.1212429109	journal	September 2012
The Structural Basis for Control of Eukaryotic Protein Kinases Endicott, Jane A.; Noble, Martin E. M.; Johnson, Louise N. Annual Review of Biochemistry, Vol. 81, Issue 1 https://doi.org/10.1146/annurev-biochem-052410-090317	journal	July 2012
Fruiting body formation by Bacillus subtilis Branda, S. S.; Gonzalez-Pastor, J. E.; Ben-Yehuda, S. Proceedings of the National Academy of Sciences, Vol. 98, Issue 20 https://doi.org/10.1073/pnas.191384198	journal	September 2001
Regulating DNA Replication in Bacteria Skarstad, K.; Katayama, T. Cold Spring Harbor Perspectives in Biology, Vol. 5, Issue 4 https://doi.org/10.1101/cshperspect.a012922	journal	March 2013
Multiple Regulatory Systems Coordinate DNA Replication with Cell Growth in Bacillus subtilis Murray, Heath; Koh, Alan PLoS Genetics, Vol. 10, Issue 10 https://doi.org/10.1371/journal.pgen.1004731	journal	October 2014
Evidence that entry into sporulation in Bacillus subtilis is governed by a gradual increase in the level and activity of the master regulator Spo0A Fujita, M. Genes & Development, Vol. 19, Issue 18 https://doi.org/10.1101/gad.1335705	journal	September 2005
In Vitro Whole Genome DNA Binding Analysis of the Bacterial Replication Initiator and Transcription Factor DnaA Smith, Janet L.; Grossman, Alan D. PLOS Genetics, Vol. 11, Issue 5 https://doi.org/10.1371/journal.pgen.1005258	journal	May 2015
A major protein component of the Bacillus subtilis biofilm matrix Branda, Steven S.; Chu, Frances; Kearns, Daniel B. Molecular Microbiology, Vol. 59, Issue 4 https://doi.org/10.1111/j.1365-2958.2005.05020.x	journal	February 2006
Bacterial single-stranded DNA-binding proteins are phosphorylated on tyrosine Mijakovic, I. Nucleic Acids Research, Vol. 34, Issue 5 https://doi.org/10.1093/nar/gkj514	journal	March 2006
Protein Flexibility Facilitates Quaternary Structure Assembly and Evolution Marsh, Joseph A.; Teichmann, Sarah A. PLoS Biology, Vol. 12, Issue 5 https://doi.org/10.1371/journal.pbio.1001870	journal	May 2014
Control of Initiation of DNA Replication in Bacillus subtilis and Escherichia coli Jameson, Katie; Wilkinson, Anthony Genes, Vol. 8, Issue 1 https://doi.org/10.3390/genes8010022	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 Jameson, Katie H.; Rostami, Nadia; Fogg, Mark J. Molecular Microbiology, Vol. 93, Issue 5 https://doi.org/10.1111/mmi.12713	journal	August 2014
Termination factor Rho: From the control of pervasive transcription to cell fate determination in Bacillus subtilis Bidnenko, Vladimir; Nicolas, Pierre; Grylak-Mielnicka, Aleksandra PLOS Genetics, Vol. 13, Issue 7 https://doi.org/10.1371/journal.pgen.1006909	journal	July 2017
Bacillus subtilis Two-Component System Sensory Kinase DegS Is Regulated by Serine Phosphorylation in Its Input Domain Jers, Carsten; Kobir, Ahasanul; Søndergaard, Elsebeth Oline PLoS ONE, Vol. 6, Issue 2 https://doi.org/10.1371/journal.pone.0014653	journal	February 2011
A novel regulatory protein governing biofilm formation in Bacillus subtilis Chu, Frances; Kearns, Daniel B.; McLoon, Anna Molecular Microbiology, Vol. 68, Issue 5 https://doi.org/10.1111/j.1365-2958.2008.06201.x	journal	June 2008
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 Vishnoi, Monika; Narula, Jatin; Devi, Seram Nganbiton Molecular Microbiology https://doi.org/10.1111/mmi.12357	journal	August 2013
Cell-Cycle-Dependent Spatial Sequestration of the DnaA Replication Initiator Protein in Bacillus subtilis Soufo, Clarisse Defeu; Soufo, Hervé Joël Defeu; Noirot-Gros, Marie-Françoise Developmental Cell, Vol. 15, Issue 6 https://doi.org/10.1016/j.devcel.2008.09.010	journal	December 2008
MoonProt: a database for proteins that are known to moonlight Mani, Mathew; Chen, Chang; Amblee, Vaishak Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku954	journal	October 2014
Genome-wide analysis of temporally regulated and compartment-specific gene expression in sporulating cells of Bacillus subtilis Steil, L. Microbiology, Vol. 151, Issue 2 https://doi.org/10.1099/mic.0.27493-0	journal	February 2005
Dynamic Association of the Replication Initiator and Transcription Factor DnaA with the Bacillus subtilis Chromosome during Replication Stress Breier, A. M.; Grossman, A. D. Journal of Bacteriology, Vol. 191, Issue 2 https://doi.org/10.1128/JB.01294-08	journal	November 2008
Bacillus subtilis YabA is involved in determining the timing and synchrony of replication initiation Hayashi, Miho; Ogura, Yoshitoshi; Harry, Elizabeth J. FEMS Microbiology Letters, Vol. 247, Issue 1 https://doi.org/10.1016/j.femsle.2005.04.028	journal	June 2005
Amyloid fibers provide structural integrity to Bacillus subtilis biofilms Romero, D.; Aguilar, C.; Losick, R. Proceedings of the National Academy of Sciences, Vol. 107, Issue 5 https://doi.org/10.1073/pnas.0910560107	journal	January 2010
SinR is a mutational target for fine-tuning biofilm formation in laboratory-evolved strains of Bacillus subtilis Leiman, Sara A.; Arboleda, Laura C.; Spina, Joseph S. BMC Microbiology, Vol. 14, Issue 1 https://doi.org/10.1186/s12866-014-0301-8	journal	November 2014
Protein synthesis during cellular quiescence is inhibited by phosphorylation of a translational elongation factor Pereira, Sandro F. F.; Gonzalez, Ruben L.; Dworkin, Jonathan Proceedings of the National Academy of Sciences, Vol. 112, Issue 25 https://doi.org/10.1073/pnas.1505297112	journal	June 2015
Catabolic repression of bacterial sporulation. Schaeffer, P.; Millet, J.; Aubert, J. P. Proceedings of the National Academy of Sciences, Vol. 54, Issue 3 https://doi.org/10.1073/pnas.54.3.704	journal	September 1965
The functional analysis of YabA, which interacts with DnaA and regulates initiation of chromosome replication in Bacillus subtils Cho, Eunha; Ogasawara, Naotake; Ishikawa, Shu Genes & Genetic Systems, Vol. 83, Issue 2 https://doi.org/10.1266/ggs.83.111	journal	January 2008
The protein kinase family: conserved features and deduced phylogeny of the catalytic domains Hanks, S.; Quinn, A.; Hunter, T. Science, Vol. 241, Issue 4861 https://doi.org/10.1126/science.3291115	journal	July 1988
Control of the replication initiator DnaA by an anti-cooperativity factor: Control of DnaA by an anti-cooperativity factor Merrikh, Houra; Grossman, Alan D. Molecular Microbiology, Vol. 82, Issue 2 https://doi.org/10.1111/j.1365-2958.2011.07821.x	journal	September 2011
Phosphorylation and functional analysis of the sporulation initiation factor Spo0A from Clostridium botulinum Worner, Kristina; Szurmant, Hendrik; Chiang, Christina Molecular Microbiology, Vol. 59, Issue 3 https://doi.org/10.1111/j.1365-2958.2005.04988.x	journal	February 2006
Protein-tyrosine phosphorylation interaction network in Bacillus subtilis reveals new substrates, kinase activators and kinase cross-talk Shi, Lei; Pigeonneau, Nathalie; Ventroux, Magali Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00538	journal	October 2014
The Primosomal Protein DnaD Inhibits Cooperative DNA Binding by the Replication Initiator DnaA in Bacillus subtilis Bonilla, Carla Y.; Grossman, Alan D. Journal of Bacteriology, Vol. 194, Issue 18 https://doi.org/10.1128/JB.00958-12	journal	July 2012
The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis: Biofilm development in Bacillus subtilis Hamon, Mélanie A.; Lazazzera, Beth A. Molecular Microbiology, Vol. 42, Issue 5 https://doi.org/10.1046/j.1365-2958.2001.02709.x	journal	December 2001
The Meiotic Checkpoint Network: Step-by-Step through Meiotic Prophase Subramanian, V. V.; Hochwagen, A. Cold Spring Harbor Perspectives in Biology, Vol. 6, Issue 10 https://doi.org/10.1101/cshperspect.a016675	journal	October 2014
Moonlighting proteins: An intriguing mode of multitasking Huberts, Daphne H. E. W.; van der Klei, Ida J. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1803, Issue 4 https://doi.org/10.1016/j.bbamcr.2010.01.022	journal	April 2010
A master regulator for biofilm formation by Bacillus subtilis: Master regulator for biofilm formation Kearns, Daniel B.; Chu, Frances; Branda, Steven S. Molecular Microbiology, Vol. 55, Issue 3 https://doi.org/10.1111/j.1365-2958.2004.04440.x	journal	December 2004
Protein species and moonlighting proteins: Very small changes in a protein's covalent structure can change its biochemical function Jeffery, Constance J. Journal of Proteomics, Vol. 134 https://doi.org/10.1016/j.jprot.2015.10.003	journal	February 2016
The DnaA inhibitor SirA acts in the same pathway as Soj (ParA) to facilitate oriC segregation during Bacillus subtilis sporulation Duan, Yi; Huey, Jack D.; Herman, Jennifer K. Molecular Microbiology, Vol. 102, Issue 3 https://doi.org/10.1111/mmi.13477	journal	August 2016
Genetic networks controlled by the bacterial replication initiator and transcription factor DnaA in Bacillus subtilis : Genes controlled by DnaA Washington, Tracy A.; Smith, Janet L.; Grossman, Alan D. Molecular Microbiology, Vol. 106, Issue 1 https://doi.org/10.1111/mmi.13755	journal	August 2017
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 Spiers, Andrew J.; Bohannon, John; Gehrig, Stefanie M. Molecular Microbiology, Vol. 50, Issue 1 https://doi.org/10.1046/j.1365-2958.2003.03670.x	journal	August 2003
YabA and DnaD inhibit helix assembly of the DNA replication initiation protein DnaA: Regulation of DnaA by YabA and DnaD Scholefield, Graham; Murray, Heath Molecular Microbiology https://doi.org/10.1111/mmi.12353	journal	August 2013
Bacillus subtilis serine/threonine protein kinase YabT is involved in spore development via phosphorylation of a bacterial recombinase Bidnenko, Vladimir; Shi, Lei; Kobir, Ahasanul Molecular Microbiology, Vol. 88, Issue 5 https://doi.org/10.1111/mmi.12233	journal	May 2013
The Spo0A regulon of Bacillus subtilis: The Spo0A regulon Molle, Virginie; Fujita, Masaya; Jensen, Shane T. Molecular Microbiology, Vol. 50, Issue 5 https://doi.org/10.1046/j.1365-2958.2003.03818.x	journal	November 2003
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 DeLoughery, Aaron; Dengler, Vanina; Chai, Yunrong Molecular Microbiology, Vol. 99, Issue 2 https://doi.org/10.1111/mmi.13240	journal	October 2015
An expanded view of bacterial DNA replication Noirot-Gros, M. -F.; Dervyn, E.; Wu, L. J. Proceedings of the National Academy of Sciences, Vol. 99, Issue 12 https://doi.org/10.1073/pnas.122040799	journal	June 2002
Role of Protein Phosphorylation in the Regulation of Cell Cycle and DNA-Related Processes in Bacteria Garcia-Garcia, Transito; Poncet, Sandrine; Derouiche, Abderahmane Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00184	journal	February 2016

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

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