Literature DB >> 29776923

Environmental Adaptability and Quorum Sensing: Iron Uptake Regulation during Biofilm Formation by Paracoccus denitrificans.

Yang Zhang1,2, Jie Gao1,2, Lushan Wang3, Shuangjiang Liu4, Zhihui Bai1,2, Xuliang Zhuang5,2, Guoqiang Zhuang5,2.   

Abstract

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.
Copyright © 2018 American Society for Microbiology.

Entities:  

Keywords:  RNA-seq; biofilm formation; iron transport system; quorum sensing

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Substances:

Year:  2018        PMID: 29776923      PMCID: PMC6029090          DOI: 10.1128/AEM.00865-18

Source DB:  PubMed          Journal:  Appl Environ Microbiol        ISSN: 0099-2240            Impact factor:   4.792


  41 in total

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Authors:  H Yamamoto; S Uchiyama; F A Nugroho; J Sekiguchi
Journal:  Gene       Date:  1997-07-31       Impact factor: 3.688

2.  LuxS involvement in the regulation of genes coding for hemin and iron acquisition systems in Porphyromonas gingivalis.

Authors:  Chloe E James; Yoshiaki Hasegawa; Yoonsuk Park; Vincent Yeung; Gena D Tribble; Masae Kuboniwa; Donald R Demuth; Richard J Lamont
Journal:  Infect Immun       Date:  2006-07       Impact factor: 3.441

Review 3.  Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators.

Authors:  W C Fuqua; S C Winans; E P Greenberg
Journal:  J Bacteriol       Date:  1994-01       Impact factor: 3.490

4.  The fbpABC locus of Neisseria gonorrhoeae functions in the periplasm-to-cytosol transport of iron.

Authors:  P Adhikari; S A Berish; A J Nowalk; K L Veraldi; S A Morse; T A Mietzner
Journal:  J Bacteriol       Date:  1996-04       Impact factor: 3.490

5.  Cloning and characterization of a gene cluster involved in the catabolism of p-nitrophenol from Pseudomonas putida DLL-E4.

Authors:  Wenjing Shen; Weidong Liu; Jing Zhang; Jian Tao; Haihua Deng; Hui Cao; Zhongli Cui
Journal:  Bioresour Technol       Date:  2010-05-13       Impact factor: 9.642

6.  The quorum-sensing transcriptional regulator TraR requires its cognate signaling ligand for protein folding, protease resistance, and dimerization.

Authors:  J Zhu; S C Winans
Journal:  Proc Natl Acad Sci U S A       Date:  2001-02-13       Impact factor: 11.205

7.  A LuxR/LuxI-type quorum-sensing system in a plant bacterium, Mesorhizobium tianshanense, controls symbiotic nodulation.

Authors:  Huiming Zheng; Zengtao Zhong; Xin Lai; Wen-Xin Chen; Shunpeng Li; Jun Zhu
Journal:  J Bacteriol       Date:  2006-03       Impact factor: 3.490

8.  The influence of iron on Pseudomonas aeruginosa physiology: a regulatory link between iron and quorum sensing.

Authors:  Amanda G Oglesby; John M Farrow; Joon-Hee Lee; Andrew P Tomaras; E P Greenberg; Everett C Pesci; Michael L Vasil
Journal:  J Biol Chem       Date:  2008-04-18       Impact factor: 5.157

9.  luxS and arcB control aerobic growth of Actinobacillus actinomycetemcomitans under iron limitation.

Authors:  Karen P Fong; Ling Gao; Donald R Demuth
Journal:  Infect Immun       Date:  2003-01       Impact factor: 3.441

10.  Investigation of quorum sensing-dependent gene expression in Burkholderia gladioli BSR3 through RNA-seq analyses.

Authors:  Sunyoung Kim; Jungwook Park; Okhee Choi; Jinwoo Kim; Young-Su Seo
Journal:  J Microbiol Biotechnol       Date:  2014-12-28       Impact factor: 2.351

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  7 in total

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2.  LC_Glucose-Inhibited Division Protein Is Required for Motility, Biofilm Formation, and Stress Response in Lysobacter capsici X2-3.

Authors:  Dan Zhao; Hong Wang; Zhiyuan Li; Shengnan Han; Chao Han; Aixin Liu
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3.  Molecular epidemiology and collaboration of siderophore-based iron acquisition with surface adhesion in hypervirulent Pseudomonas aeruginosa isolates from wound infections.

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4.  Indole-Acetic Acid Promotes Ammonia Removal Through Heterotrophic Nitrification, Aerobic Denitrification With Mixed Enterobacter sp. Z1 and Klebsiella sp. Z2.

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

Authors:  Na Wang; Jie Gao; Shujie Xiao; Guoqiang Zhuang
Journal:  Front Microbiol       Date:  2022-08-10       Impact factor: 6.064

6.  Ecological Role of Volatile Organic Compounds Emitted by Pantoea agglomerans as Interspecies and Interkingdom Signals.

Authors:  Maria Vasseur-Coronado; Anthi Vlassi; Hervé Dupré du Boulois; Rainer Schuhmacher; Alexandra Parich; Ilaria Pertot; Gerardo Puopolo
Journal:  Microorganisms       Date:  2021-05-31

7.  The substrate-dependent regulatory effects of the AfeI/R system in Acidithiobacillus ferrooxidans reveals the novel regulation strategy of quorum sensing in acidophiles.

Authors:  Xue-Yan Gao; Chang-Ai Fu; Likai Hao; Xiu-Feng Gu; Rui Wang; Jian-Qiang Lin; Xiang-Mei Liu; Xin Pang; Cheng-Jia Zhang; Jian-Qun Lin; Lin-Xu Chen
Journal:  Environ Microbiol       Date:  2020-08-02       Impact factor: 5.491

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