Far from being well understood: multiple protein phosphorylation events control cell differentiation in Bacillus subtilis at different levels

Gerwig, Jan; Stülke, Jörg

doi:10.3389/fmicb.2014.00704

Cited by 6 publications

(8 citation statements)

References 34 publications

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“…In B. subtilis, the BY-kinase and the kinase activators, EpsB and EpsA, are involved in the regulation of EPS biosynthesis and biofilm formation (44,46,49). Previous studies also suggested that the second BY-kinase PtkA, augments the role of EpsB in biofilm formation (44,52).…”

Section: Discussionmentioning

confidence: 99%

“…The biological functions of TkmA, PtkA, and PtpZ have been investigated in previous studies. It was shown that the protein targets of the PtkA kinase include Ugd and TuaD (involved in teichuronic acid biosynthesis), as well as the single-strand DNA-binding proteins SsbA and SsbB (45,49,51). Recent studies also indicated the roles of TkmA and PtkA in biofilm formation.…”

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confidence: 97%

“…subtilis also possesses a second BY-kinase-kinase activator pair, PtkA and TkmA, respectively (45,49). The genes for the two proteins are located in a presumptive operon with two other genes, ptpZ and ugd (Fig.…”

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confidence: 99%

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The Bacterial Tyrosine Kinase Activator TkmA Contributes to Biofilm Formation Largely Independently of the Cognate Kinase PtkA in Bacillus subtilis

Gao

Greenwich

et al. 2015

J Bacteriol

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In Bacillus subtilis, biosynthesis of exopolysaccharide (EPS), a key biofilm matrix component, is regulated at the posttranslational level by the bacterial tyrosine kinase (BY-kinase) EpsB. EpsB, in turn, relies on the cognate kinase activator EpsA for activation. A concerted role of a second BY-kinase-kinase activator pair, PtkA and TkmA, respectively in biofilm formation was also indicated in previous studies. However, the exact functions of PtkA and TkmA in biofilm formation remain unclear. In this work, we show that the kinase activator TkmA contributes to biofilm formation largely independently of the cognate kinase, PtkA. We further show that the biofilm defect caused by a ⌬tkmA mutation can be rescued by complementation by epsA, suggesting a functional overlap between TkmA and EpsA and providing a possible explanation for the role of TkmA in biofilm formation. We also show that the importance of TkmA in biofilm formation depends largely on medium conditions; the biofilm defect of ⌬tkmA is very severe in the biofilm medium LBGM (lysogenic broth M thiamine, 0.5% glycerol, 0.5% glutamic acid, 50 g/ml tryptophan, 50 g/ml threonine, and 50 g/ml phenylalanine). The molecular basis for the medium dependence is likely due to differential expression of tkmA and epsA in the two different media and complex regulation of these genes by both Spo0A and DegU. Our studies provide genetic evidence for possible cross talk between a BY-kinase activator (TkmA) and a noncognate kinase (EpsB) and an example of how environmental conditions may influence such cross talk in regulating biofilm formation in B. subtilis.[ IMPORTANCEIn bacteria, biosynthesis of secreted polysaccharides is often regulated by bacterial tyrosine kinases (BY-kinases). BY-kinases, in turn, rely on cognate kinase activators for activation. In this study, we investigated the role of a BY-kinase activator in biofilm formation in Bacillus subtilis. We present evidence that different BY-kinase activators may functionally overlap each other, as well as an example of how activities of the BY-kinase activators may be highly dependent on environmental conditions. Our study broadens the understanding of the complexity of regulation of the BY-kinases/kinase activators and the influence on bacterial cell physiology. Biofilms are multicellular communities of bacteria with highly complex structures and distinct morphological features (1-4). One of the most important characteristics of biofilms is the presence of a self-produced extracellular matrix, which allows individual cells within the biofilm to stick to each other (2, 3, 5). In Bacillus subtilis, the biofilm matrix consists of an exopolysaccharide (EPS); the amyloid fiber-like protein TasA; and a small hydrophobin, BslA (6-11). The regulatory circuit that controls the expression of the matrix-encoding genes has been well studied in B. subtilis (5,(12)(13)(14). EPS and TasA fibers are produced by the protein products of two matrix operons, epsA-epsO and tapA-sipW-tasA, respectively (8, 15). These two opero...

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Section: Discussionmentioning

confidence: 99%

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confidence: 97%

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The Bacterial Tyrosine Kinase Activator TkmA Contributes to Biofilm Formation Largely Independently of the Cognate Kinase PtkA in Bacillus subtilis

Gao

Greenwich

et al. 2015

J Bacteriol

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“…This approach for reconstructing phosphorylation networks highlights the capacity of bacterial proteins kinases from different families to interact with, and phosphorylate, each other (Shi et al, 2014b). Protein-tyrosine kinases, and their various roles in bacterial physiology were in the focus of several review and opinion articles in this topic (Barák, 2014;Gerwig and Stülke, 2014;Mijakovic and Deutscher, 2015).…”

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confidence: 99%

Regulatory Potential of Post-translational Modifications in Bacteria

2015

Frontiers Research Topics

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“…The biological function of TkmA, PtkA, and PtpZ have been investigated in previous studies. It was shown that the protein targets of the PtkA kinase include Ugd, TuaD (involved in teichuronic acid biosynthesis) as well as single strand DNA-binding proteins SsbA and SsbB [121,124,125].…”

Section: Introductionmentioning

confidence: 99%

Novel signaling mechanisms regulating biofilm formation in Bacillus subtilis

Greenwich¹

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Associate Professor of Biology would not be where I am today without all of you. To the LONG squad (past and present) -thank you for letting a scientist be a history nerd and play lawn games all these years. It means the world to me. To the many friends I made along the way-thank you for the love and support you have given me over the years. Dan-thanks for starting so many conversations we'll never finish, giving me an excuse to leave the lab, and of course, introducing me to my favorite brothers that I am not related to. I never would have gotten through grad school without them. To John and Hank Green, for never forgetting to be awesome and giving me an escape from grad school. To Hank, thank you for helping me identify what my passions are and being an inspirational science communicator.Finally, and most importantly, thank you to my family. Your unconditional love and support has brought me to where I am and I could not have done it without you. This degree belongs as much to you as it does to me, if not more so. Mom-you never let me give up, and I don't tell you often enough how much I appreciate that. Aunt Marge-thank you for everything you've done to support me all of these years. Joe-thanks for keeping me humble and reminding me to be normal. Sorry I'll never remember. Abstract of DissertationBacteria are capable of forming multicellular communities, known as biofilms. Bacillus subtilis is a Gram-positive, rod shaped, soil-dwelling bacterium often used as a model organism to study biofilm formation. Both extracellular and intracellular signals can trigger biofilm formation through a signaling cascade, which turns on genes involved in production of the biofilm matrix. In B. subtilis, the matrix consists of an exopolysaccharide (EPS) component and two protein components, which are regulated on a genetic level by two master regulators, SinR and AbrB.Biosynthesis of the EPS is also regulated at the post-translational level, by a bacterial tyrosine kinase (BY-kinase), EpsB, which is encoded within the same operon as the enzymes involved in the biosynthesis of EPS. EpsB is activated by EpsA, which senses EPS in a quorum-sensing-like manner. We show genetic evidence for EpsB activation by TkmA, a modulator of a different BYkinase can activate EpsB. This cross-talk allows B. subtilis to increase the signals to which it can respond.Intracellularly, serine starvation triggers biofilm formation. We elucidate the mechanism by which this occurs and investigate the regulation of serine biosynthesis. Expression of serA, which encodes SerA, the enzyme responsible for the first and rate-limiting step of serine biosynthesis decreases upon entry into stationary phase and is regulated by catabolite control. This regulation allows cells to trigger biofilm formation based on available nutrients as well as external stimuli.Accompanying this decrease in serine is a decrease in seryl-tRNA isoacceptors, responsible for adding serine to growing peptide chains in the ribosome. It was previously observed that ribosomes pause on specif...

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Far from being well understood: multiple protein phosphorylation events control cell differentiation in Bacillus subtilis at different levels

Cited by 6 publications

References 34 publications

The Bacterial Tyrosine Kinase Activator TkmA Contributes to Biofilm Formation Largely Independently of the Cognate Kinase PtkA in Bacillus subtilis

The Bacterial Tyrosine Kinase Activator TkmA Contributes to Biofilm Formation Largely Independently of the Cognate Kinase PtkA in Bacillus subtilis

Regulatory Potential of Post-translational Modifications in Bacteria

Novel signaling mechanisms regulating biofilm formation in Bacillus subtilis

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