Phosphorylation of the Bacillus subtilis Replication Controller YabA Plays a Role in Regulation of Sporulation and Biofilm Formation
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 wi...
Main Authors: | , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Frontiers Media S.A.
2018-03-01
|
Series: | Frontiers in Microbiology |
Subjects: | |
Online Access: | http://journal.frontiersin.org/article/10.3389/fmicb.2018.00486/full |
_version_ | 1828427389193945088 |
---|---|
author | Tránsito García García Magali Ventroux Abderahmane Derouiche Vladimir Bidnenko Sara Correia Santos Céline Henry Ivan Mijakovic Marie-Françoise Noirot-Gros Sandrine Poncet |
author_facet | Tránsito García García Magali Ventroux Abderahmane Derouiche Vladimir Bidnenko Sara Correia Santos Céline Henry Ivan Mijakovic Marie-Françoise Noirot-Gros Sandrine Poncet |
author_sort | Tránsito García García |
collection | DOAJ |
description | 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. 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. |
first_indexed | 2024-12-10T17:01:04Z |
format | Article |
id | doaj.art-febfea72e9384a938b02898f56c34ec2 |
institution | Directory Open Access Journal |
issn | 1664-302X |
language | English |
last_indexed | 2024-12-10T17:01:04Z |
publishDate | 2018-03-01 |
publisher | Frontiers Media S.A. |
record_format | Article |
series | Frontiers in Microbiology |
spelling | doaj.art-febfea72e9384a938b02898f56c34ec22022-12-22T01:40:34ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-03-01910.3389/fmicb.2018.00486341198Phosphorylation of the Bacillus subtilis Replication Controller YabA Plays a Role in Regulation of Sporulation and Biofilm FormationTránsito García García0Magali Ventroux1Abderahmane Derouiche2Vladimir Bidnenko3Sara Correia Santos4Céline Henry5Ivan Mijakovic6Marie-Françoise Noirot-Gros7Sandrine Poncet8Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, FranceMicalis Institute, INRA, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, FranceSystems and Synthetic Biology, Chalmers University of Technology, Göteborg, SwedenMicalis Institute, INRA, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, FranceMicalis Institute, INRA, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, FranceMicalis Institute, INRA, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, FranceSystems and Synthetic Biology, Chalmers University of Technology, Göteborg, SwedenArgonne National Laboratory, Biosciences Division, Argonne, IL, United StatesMicalis Institute, INRA, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, FranceBacillus 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. 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.http://journal.frontiersin.org/article/10.3389/fmicb.2018.00486/fullBacillus subtilisSer/Thr kinasesporulationbiofilmreplication initiation control |
spellingShingle | Tránsito García García Magali Ventroux Abderahmane Derouiche Vladimir Bidnenko Sara Correia Santos Céline Henry Ivan Mijakovic Marie-Françoise Noirot-Gros Sandrine Poncet Phosphorylation of the Bacillus subtilis Replication Controller YabA Plays a Role in Regulation of Sporulation and Biofilm Formation Frontiers in Microbiology Bacillus subtilis Ser/Thr kinase sporulation biofilm replication initiation control |
title | Phosphorylation of the Bacillus subtilis Replication Controller YabA Plays a Role in Regulation of Sporulation and Biofilm Formation |
title_full | Phosphorylation of the Bacillus subtilis Replication Controller YabA Plays a Role in Regulation of Sporulation and Biofilm Formation |
title_fullStr | Phosphorylation of the Bacillus subtilis Replication Controller YabA Plays a Role in Regulation of Sporulation and Biofilm Formation |
title_full_unstemmed | Phosphorylation of the Bacillus subtilis Replication Controller YabA Plays a Role in Regulation of Sporulation and Biofilm Formation |
title_short | Phosphorylation of the Bacillus subtilis Replication Controller YabA Plays a Role in Regulation of Sporulation and Biofilm Formation |
title_sort | phosphorylation of the bacillus subtilis replication controller yaba plays a role in regulation of sporulation and biofilm formation |
topic | Bacillus subtilis Ser/Thr kinase sporulation biofilm replication initiation control |
url | http://journal.frontiersin.org/article/10.3389/fmicb.2018.00486/full |
work_keys_str_mv | AT transitogarciagarcia phosphorylationofthebacillussubtilisreplicationcontrolleryabaplaysaroleinregulationofsporulationandbiofilmformation AT magaliventroux phosphorylationofthebacillussubtilisreplicationcontrolleryabaplaysaroleinregulationofsporulationandbiofilmformation AT abderahmanederouiche phosphorylationofthebacillussubtilisreplicationcontrolleryabaplaysaroleinregulationofsporulationandbiofilmformation AT vladimirbidnenko phosphorylationofthebacillussubtilisreplicationcontrolleryabaplaysaroleinregulationofsporulationandbiofilmformation AT saracorreiasantos phosphorylationofthebacillussubtilisreplicationcontrolleryabaplaysaroleinregulationofsporulationandbiofilmformation AT celinehenry phosphorylationofthebacillussubtilisreplicationcontrolleryabaplaysaroleinregulationofsporulationandbiofilmformation AT ivanmijakovic phosphorylationofthebacillussubtilisreplicationcontrolleryabaplaysaroleinregulationofsporulationandbiofilmformation AT mariefrancoisenoirotgros phosphorylationofthebacillussubtilisreplicationcontrolleryabaplaysaroleinregulationofsporulationandbiofilmformation AT sandrineponcet phosphorylationofthebacillussubtilisreplicationcontrolleryabaplaysaroleinregulationofsporulationandbiofilmformation |