Publikationsserver der Universitätsbibliothek Marburg

Titel: The role of the second messenger cyclic di-GMP in Bacillus subtilis
Autor: Bedrunka, Patricia
Weitere Beteiligte: Graumann, Peter L. (Prof. Dr.)
Veröffentlicht: 2017
URI: https://archiv.ub.uni-marburg.de/diss/z2017/0538
URN: urn:nbn:de:hebis:04-z2017-05384
DOI: https://doi.org/10.17192/z2017.0538
DDC: 540 Chemie
Titel(trans.): Die Role des sekundären Botenstoffes zyklisches di-GMP in Bacillus subtilis
Publikationsdatum: 2018-02-28
Lizenz: https://rightsstatements.org/vocab/InC-NC/1.0/

Dokument

Schlagwörter:
Bacillus, GGDEF Proteine, zyklisches di-GMP, Botenstoff, cyclic di-GMP, Biofilm, GGDEF proteins

Summary:
The bacterial second messenger c-di-GMP represents an integral key regulator in the control of bacterial motility and biofilm formation. In this context, an increase in intracellular c-di-GMP production correlates with a sessile lifestyle, whereas low c-di-GMP levels favor planktonic cell behavior. Intracellular c-di-GMP levels are controlled by the antagonistic activity of c-di-GMP specific synthetases (diguanylate cyclases, DGCs) and hydrolases (phosphodiesterases, PDEs). Bacteria contain diverse c-di-GMP binding receptors/effectors, which exert the regulatory functions of this signaling molecule. A given bacterial genome typically encodes several paralogous copies of DGCs and PDEs. This lead to the question of how cells cope with such a multiplicity of signaling components and guarantee that specificity within certain signaling modules is mediated. Two general models for signal specificity through functional sequestration are currently discussed: the so-called local and global pool signaling hypotheses. Spatially sequestering the signal (pool) in multi-protein complexes at distinct cellular site may result in highly specific signaling pathways. Temporal and/ or conditional separation through differential expression and activation of DGCs/ PDEs/ output systems respectively, could have a distinct impact on the global c-di-GMP pool. This work investigates the role of c-di-GMP and its players in the Gram-positive model organism B. subtilis, which possesses a relatively small c-di-GMP signaling equipment. In particular, the obtained findings define a novel c-di-GMP signaling pathway regulating the production of an unknown exopolysaccharide (EPS) and furthermore imply that local and global signaling pools potentially operate in B. subtilis to regulate motility and exopolysaccharide production. The proposed c-di-GMP receptor YdaK resides in the putative EPS synthesis operon ydaJKLMN. Artificial YdaJ-N induction results in strongly altered colony biofilms, increased Congo Red staining and provokes furthermore cell clumping, which provides indirect evidence of EPS production. The putative EPS synthase components YdaM/ YdaN and YdaK co-localize to clusters predominantly at the cell poles and are statically positioned at this subcellular site, suggesting that exopolysaccharide production takes place at distinct sites of the membrane. The potential glycosyl hydrolase YdaJ is not essential for the generation of the above-described phenotypes, whereas the presence of YdaK is required, implying an involvement of the second messenger c-di-GMP. To approach the potential regulation of exopolysaccharide production through c-di-GMP via YdaK, different combinations of overexpression and deletion mutants of the operon and of dgc genes, respectively, were generated. Importantly, the presence of dgcK was shown to be indispensable for the production of the unknown EPS, thereby revealing a new function for one of the three known DGC enzymes. DgcK and YdaK partially co-localize to the same subcellular positions at the cell membrane implying close proximity of these players, which strongly suggests that YdaK receives its activation signal directly from the spatially close DgcK in agreement with the local pool hypothesis. The cytoplasmic DgcP synthetase can complement for DgcK only upon overproduction, while the third c-di-GMP synthetase, DgcW, seems not to be part of the signaling pathway. Removal of the regulatory EAL domain from DgcW reveals a distinct function in biofilm formation. Therefore, our study is compatible with the local pool signaling hypothesis, but shows that in case of the yda operon, this can easily be overcome by overproduction of non-cognate DGCs, indicating that global pools can also confer signals to this regulatory circuit. Furthermore, indications are provided within this study that all three DGCs might cooperate in inhibition of motility via the c-di-GMP receptor DgrA indicating that DgrA depends on globally elevated c-di-GMP levels.

Zusammenfassung:
Der bakterielle sekundäre Botenstoff c-di-GMP repräsentiert einen integralen Schlüsselregler in der Kontrolle der bakteriellen Motilität und der Biofilmbildung. In diesem Zusammenhang korreliert eine Zunahme der intrazellulären c-di-GMP-Produktion mit einer sessilen Lebensweise, während niedrige c-di-GMP-Spiegel planktonisches Zellverhalten begünstigen. Die intrazelluläre c-di-GMP-Menge wird durch die antagonistische Aktivität von c-di-GMP-spezifischen Synthetasen (Diguanylatzyklasen, DGCs) und Hydrolasen (Phosphodiesterasen, PDEs) gesteuert. Bakterien besitzen verschiedene c-di-GMP-Bindungsrezeptoren/ Effektoren, welche die regulatorischen Funktionen dieses Signalmoleküls ausüben. Ein gegebenes bakterielles Genom kodiert typischerweise mehrere paralogische Kopien von DGCs und PDEs. Dies führt zu der Frage, wie Zellen mit einer solchen Vielzahl von Signalkomponenten zurechtkommen und garantieren, dass Spezifität innerhalb bestimmter Signalmodule vermittelt wird. Zwei allgemeine Modelle für die Signalspezifität durch funktionelle Sequestrierung werden derzeit diskutiert: die sogenannten lokalen und globalen Pool-Signal-Hypothesen. Die räumliche Sequestrierung des Signals (Pool) in Multi-Protein-Komplexe an einer bestimmten zellulären Stelle kann zu hochspezifischen Signalwegen führen. Die zeitliche und/ oder konditionale Trennung durch differentielle Expression und Aktivierung von DGCs/PDEs/ Output-Systemen könnte einen deutlicheren Einfluss auf den globalen c-di-GMP-Pool haben. Die vorliegende Arbeit untersucht die Rolle von c-di-GMP und seinen Spielern im Gram-positiven Modellorganismus B. subtilis, welcher eine relativ kleine c-di-GMP-Signalausrüstung aufweist. Insbesondere definieren die erhaltenen Erkenntnisse einen neuen c-di-GMP-Signalweg, der die Produktion eines unbekannten Exopolysaccharids (EPSs) reguliert. Darüber hinaus implizieren die erhaltenen Ergebnisse, dass lokale und globale Signalpools potentiell in B. subtilis operieren, um Motilität und EPS-Produktion zu regulieren. Der vorgeschlagene c-di-GMP-Rezeptor YdaK ist in dem putativen EPS-Operon ydaJKLMN kodiert. Eine künstliche YdaJ-N Induktion führt zu stark veränderten Kolonie-Biofilmen, einer erhöhten Kongo-Rot-Färbung und provoziert darüber hinaus Zellverklumpungen. Diese Beobachtungen liefern indirekte Beweise für die Produktion eines EPSs. Die mutmaßlichen EPS-Synthasekomponenten YdaM/ YdaN und YdaK co-lokalisieren vorwiegend an den Zellpolen als Cluster und sind an diesen subzellulären Stellen statisch positioniert. Dies deutet darauf hin, dass die EPS-Produktion an bestimmten Positionen der Membran stattfindet. Die potentielle Glykosylhydrolase YdaJ ist für die Erzeugung der oben beschriebenen Phänotypen nicht essentiell, während die Anwesenheit von YdaK erforderlich ist, was auf eine Beteiligung des sekundären Botenstoffs c-di-GMP hindeutet. Um die potenzielle Regulierung der EPS-Produktion durch c-di-GMP über YdaK zu untersuchen, wurden unterschiedliche Kombinationen von Überexpressions- und Deletionsmutanten des Operons bzw. von dgc Genen erzeugt. Wichtig ist, dass die Anwesenheit von dgcK für die Herstellung des unbekannten EPSs unentbehrlich war und damit eine neue Funktion für eines der drei bekannten DGC-Enzyme enthüllt wurde. DgcK und YdaK co-lokalisieren partiell an den gleichen subzellulären Positionen der Zellmembran. Dies impliziert eine direkte Nähe der Spieler und deutet in Übereinstimmung mit der lokalen Poolhypothese darauf hin, dass YdaK sein Aktivierungssignal direkt von der räumlich nahen DgcK erhält. Die zytoplasmatische DgcP-Synthetase kann DgcK durch Überproduktion komplementieren, während die dritte c-di-GMP-Synthetase, DgcW, nicht Teil des Signalweges zu sein scheint. Eine Entfernung der regulatorischen EAL-Domäne von DgcW zeigt eine andere Funktion im Bezug auf Biofilmbildung auf. Daher ist diese Studie kompatibel mit der lokalen Pool-Signal-Hypothese, zeigt aber, dass im Falle des Yda-Operons dies leicht durch Überproduktion von nicht-verwandten DGCs überwunden werden kann, sodass globale Pools vermutlich auch Signale an diese regulatorische Schaltung vermitteln können. Darüber hinaus werden in dieser Studie Hinweise vorgelegt, dass alle drei DGCs an der Hemmung der Motilität über den c-di-GMP-Rezeptor DgrA beteiligt sein könnten, was darauf hinweist, dass DgrA von global erhöhten c-di-GMP Konzentrationen abhängt.

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