Dataset Information

Overexpression of pdeR promotes biofilm formation of Paracoccus denitrificans by promoting ATP production and iron acquisition.

ABSTRACT: Bacterial biofilms are ubiquitous in natural environments and play an essential role in bacteria's environmental adaptability. Quorum sensing (QS), as the main signaling mechanism bacteria used for cell-to-cell communication, plays a key role in bacterial biofilm formation. However, little is known about the role of QS circuit in the N-transformation type strain, Paracoccus denitrificans, especially for the regulatory protein PdeR. In this study, we found the overexpression of pdeR promoted bacterial aggregation and biofilm formation. Through RNA-seq analysis, we demonstrated that PdeR is a global regulator which could regulate 656 genes expression, involved in multiple metabolic pathways. Combined with transcriptome as well as biochemical experiments, we found the overexpressed pdeR mainly promoted the intracellular degradation of amino acids and fatty acids, as well as siderophore biosynthesis and transportation, thus providing cells enough energy and iron for biofilm development. These results revealed the underlying mechanism for PdeR in biofilm formation of P. denitrificans, adding to our understanding of QS regulation in biofilm development.

SUBMITTER: Wang N

PROVIDER: S-EPMC9399729 | biostudies-literature | 2022

REPOSITORIES: biostudies-literature

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Overexpression of pdeR promotes biofilm formation of Paracoccus denitrificans by promoting ATP production and iron acquisition.

Wang Na N Gao Jie J Xiao Shujie S Zhuang Guoqiang G

Frontiers in microbiology 20220810

Bacterial biofilms are ubiquitous in natural environments and play an essential role in bacteria's environmental adaptability. Quorum sensing (QS), as the main signaling mechanism bacteria used for cell-to-cell communication, plays a key role in bacterial biofilm formation. However, little is known about the role of QS circuit in the N-transformation type strain, Paracoccus denitrificans, especially for the regulatory protein PdeR. In this study, we found the overexpression of pdeR ...[more]

PMID: 36033861

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Project description:Paracoccus denitrificans is a valuable model organism due to its versatile respiration capability and bioenergetic flexibility, both of which are critical to its survival in different environments. Quorum sensing (QS) plays a crucial role in the regulation of many cell functions; however, whether QS systems play a role in P. denitrificans is unknown. In this study, we demonstrated that iron uptake systems in P. denitrificans were directly regulated by a newly identified QS system. Genes coding for TonB-dependent systems, which transport chelated iron, were transcribed at higher levels in the QS-defective mutants. In contrast, genes coding for the Fbp system, which is TonB independent and transports unchelated ferric iron, were downregulated in the mutants. In brief, QS in P. denitrificans triggers a switch in iron uptake from TonB-dependent to TonB-independent transport during biofilm formation as higher concentrations of iron accumulate in the exopolysaccharide (EPS). Switching from TonB-dependent iron uptake systems to TonB-independent systems not only prevents cells from absorbing excess iron but also conserves energy. Our data suggest that iron uptake strategies are directly regulated by QS in Paracoccus denitrificans to support their survival in available ecological niches.IMPORTANCE As iron is an important trace metal for most organisms, its absorption is highly regulated. Fur has been reported as a prevalent regulator of iron acquisition. In addition, there is a relationship between QS and iron acquisition in pathogenic microbes. However, there have been few studies on the iron uptake strategies of nonpathogenic bacteria. In this study, we demonstrated that iron uptake systems in Paracoccus denitrificans PD1222 were regulated by a newly identified PdeR/PdeI QS system during biofilm formation, and we put forward a hypothesis that QS-dependent iron uptake systems benefit the stability of biofilms. This report elaborates the correlation among QS, iron uptake, and biofilm formation and thus contributes to an understanding of the ecological behavior of environmental bacteria.

Project description:Iron (Fe) is the most important metal in biology. Despite its abundance, Fe is mostly present as a ferric form in soils, strongly limiting its bioavailability. To overcome the challenge of Fe acquisition, many microorganisms produce siderophores to retrieve Fe from natural sources. Another ubiquitous feature of bacteria in natural environments is biofilm formation. Previous studies showed that external Fe strongly influenced biofilm formation in several bacteria, suggesting that this microenvironment plays a mechanistic role in micronutrient acquisition for bacteria. Here, we applied a complementary set of analytical methods and deletion mutants to evaluate the role of biofilm formation, siderophore production, and their interaction in Fe homeostasis in Bacillus subtilis We observed that Fe homeostasis, i.e., active growth at a constant intracellular Fe concentration, requires both siderophore production and biofilm formation. Also, we report that in B. subtilis, both biofilm formation and siderophore production are required to achieve active Fe acquisition from the medium and to sustain normal growth. Furthermore, we provide evidence that the formation of biofilm slightly enhances the kinetics of Fe complexation by catechol siderophores and markedly improves siderophore use efficiency. These results provide new perspectives on the mechanism underlying siderophore-based acquisition of Fe in biofilm-forming bacteria.IMPORTANCE Iron acquisition is of fundamental importance for microorganisms, since this metal is generally poorly bioavailable under natural conditions. In the environment, most bacteria are found tightly packed within multicellular communities named biofilms. Here, using the soil Gram-positive bacterium Bacillus subtilis, we show that biofilm formation and the production of siderophores, i.e., small molecules specifically binding metals, are both essential to ensure Fe uptake from the medium and maintain cellular Fe homeostasis. The biofilm matrix appears to play an important role favoring the efficient usage of siderophores. Taken together, our results demonstrate a close link between biofilm formation and iron acquisition in B. subtilis, allowing a better comprehension of how bacteria can cope with metal limitation under environmental conditions.

Dataset Information

Overexpression of pdeR promotes biofilm formation of Paracoccus denitrificans by promoting ATP production and iron acquisition.

Publications

Overexpression of <i>pdeR</i> promotes biofilm formation of <i>Paracoccus denitrificans</i> by promoting ATP production and iron acquisition.

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