The MapZ-Mediated Methylation of Chemoreceptors Contributes to Pathogenicity of Pseudomonas aeruginosa

The pathogenic bacterium Pseudomonas aeruginosa is notorious for causing acute and chronic infections in humans. The ability to infect host by P. aeruginosa is dependent on a complex cellular signaling network, which includes a large number of chemosensory signaling pathways that rely on the methyl-...

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Main Authors: Shuo Sheng, Lingyi Xin, Joey Kuok Hoong Yam, May Margarette Salido, Nicole Zi Jia Khong, Qiong Liu, Rachel Andrea Chea, Hoi Yeung Li, Liang Yang, Zhao-Xun Liang, Linghui Xu
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-02-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.00067/full
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author Shuo Sheng
Shuo Sheng
Lingyi Xin
Lingyi Xin
Joey Kuok Hoong Yam
Joey Kuok Hoong Yam
Joey Kuok Hoong Yam
May Margarette Salido
May Margarette Salido
May Margarette Salido
Nicole Zi Jia Khong
Qiong Liu
Qiong Liu
Rachel Andrea Chea
Hoi Yeung Li
Liang Yang
Liang Yang
Liang Yang
Zhao-Xun Liang
Zhao-Xun Liang
Linghui Xu
Linghui Xu
author_facet Shuo Sheng
Shuo Sheng
Lingyi Xin
Lingyi Xin
Joey Kuok Hoong Yam
Joey Kuok Hoong Yam
Joey Kuok Hoong Yam
May Margarette Salido
May Margarette Salido
May Margarette Salido
Nicole Zi Jia Khong
Qiong Liu
Qiong Liu
Rachel Andrea Chea
Hoi Yeung Li
Liang Yang
Liang Yang
Liang Yang
Zhao-Xun Liang
Zhao-Xun Liang
Linghui Xu
Linghui Xu
author_sort Shuo Sheng
collection DOAJ
description The pathogenic bacterium Pseudomonas aeruginosa is notorious for causing acute and chronic infections in humans. The ability to infect host by P. aeruginosa is dependent on a complex cellular signaling network, which includes a large number of chemosensory signaling pathways that rely on the methyl-accepting chemotaxis proteins (MCPs). We previously found that the second messenger c-di-GMP-binding adaptor MapZ modulates the methylation of an amino acid-detecting MCP by directly interacting with a chemotaxis methyltransferase CheR1. The current study further expands our understanding of the role of MapZ in regulating chemosensory pathways by demonstrating that MapZ suppresses the methylation of multiple MCPs in P. aeruginosa PAO1. The MCPs under the control of MapZ include five MCPs (Aer, CtpH, CptM, PctA, and PctB) for detecting oxygen/energy, inorganic phosphate, malate and amino acids, and three MCPs (PA1251, PA1608, and PA2867) for detecting unknown chemoattractant or chemorepellent. Chemotaxis assays showed that overexpression of MapZ hampered the taxis of P. aeruginosa toward chemoattractants and scratch-wounded human cells. Mouse infection experiments demonstrated that a dysfunction in MapZ regulation had a profound negative impact on the dissemination of P. aeruginosa and resulted in attenuated bacterial virulence. Together, the results imply that by controlling the methylation of various MCPs via the adaptor protein MapZ, c-di-GMP exerts a profound influence on chemotactic responses and bacterial pathogenesis.
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spelling doaj.art-a4a19e7637e5422980bb6cd4b877bbe32022-12-22T01:00:02ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-02-011010.3389/fmicb.2019.00067427655The MapZ-Mediated Methylation of Chemoreceptors Contributes to Pathogenicity of Pseudomonas aeruginosaShuo Sheng0Shuo Sheng1Lingyi Xin2Lingyi Xin3Joey Kuok Hoong Yam4Joey Kuok Hoong Yam5Joey Kuok Hoong Yam6May Margarette Salido7May Margarette Salido8May Margarette Salido9Nicole Zi Jia Khong10Qiong Liu11Qiong Liu12Rachel Andrea Chea13Hoi Yeung Li14Liang Yang15Liang Yang16Liang Yang17Zhao-Xun Liang18Zhao-Xun Liang19Linghui Xu20Linghui Xu21Guangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Centre, South China Agricultural University, Guangzhou, ChinaGuangdong Innovative and Entrepreneurial Research Team of Sociomicrobiology, South China Agricultural University, Guangzhou, ChinaSchool of Biological Sciences, Nanyang Technological University, Singapore, SingaporeSingapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore, SingaporeSchool of Biological Sciences, Nanyang Technological University, Singapore, SingaporeSingapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore, SingaporeInterdisciplinary Graduate School, Nanyang Technological University, Singapore, SingaporeSchool of Biological Sciences, Nanyang Technological University, Singapore, SingaporeSingapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore, SingaporeInterdisciplinary Graduate School, Nanyang Technological University, Singapore, SingaporeSchool of Biological Sciences, Nanyang Technological University, Singapore, SingaporeGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Centre, South China Agricultural University, Guangzhou, ChinaGuangdong Innovative and Entrepreneurial Research Team of Sociomicrobiology, South China Agricultural University, Guangzhou, ChinaSchool of Biological Sciences, Nanyang Technological University, Singapore, SingaporeSchool of Biological Sciences, Nanyang Technological University, Singapore, SingaporeSchool of Biological Sciences, Nanyang Technological University, Singapore, SingaporeSingapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore, SingaporeInterdisciplinary Graduate School, Nanyang Technological University, Singapore, SingaporeSchool of Biological Sciences, Nanyang Technological University, Singapore, SingaporeSingapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore, SingaporeGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Centre, South China Agricultural University, Guangzhou, ChinaGuangdong Innovative and Entrepreneurial Research Team of Sociomicrobiology, South China Agricultural University, Guangzhou, ChinaThe pathogenic bacterium Pseudomonas aeruginosa is notorious for causing acute and chronic infections in humans. The ability to infect host by P. aeruginosa is dependent on a complex cellular signaling network, which includes a large number of chemosensory signaling pathways that rely on the methyl-accepting chemotaxis proteins (MCPs). We previously found that the second messenger c-di-GMP-binding adaptor MapZ modulates the methylation of an amino acid-detecting MCP by directly interacting with a chemotaxis methyltransferase CheR1. The current study further expands our understanding of the role of MapZ in regulating chemosensory pathways by demonstrating that MapZ suppresses the methylation of multiple MCPs in P. aeruginosa PAO1. The MCPs under the control of MapZ include five MCPs (Aer, CtpH, CptM, PctA, and PctB) for detecting oxygen/energy, inorganic phosphate, malate and amino acids, and three MCPs (PA1251, PA1608, and PA2867) for detecting unknown chemoattractant or chemorepellent. Chemotaxis assays showed that overexpression of MapZ hampered the taxis of P. aeruginosa toward chemoattractants and scratch-wounded human cells. Mouse infection experiments demonstrated that a dysfunction in MapZ regulation had a profound negative impact on the dissemination of P. aeruginosa and resulted in attenuated bacterial virulence. Together, the results imply that by controlling the methylation of various MCPs via the adaptor protein MapZ, c-di-GMP exerts a profound influence on chemotactic responses and bacterial pathogenesis.https://www.frontiersin.org/article/10.3389/fmicb.2019.00067/fullPseudomonas aeruginosachemotaxisPilZ adaptorcyclic di-GMPmethyl-accepting chemotaxis proteinmethyltransferase cheR1
spellingShingle Shuo Sheng
Shuo Sheng
Lingyi Xin
Lingyi Xin
Joey Kuok Hoong Yam
Joey Kuok Hoong Yam
Joey Kuok Hoong Yam
May Margarette Salido
May Margarette Salido
May Margarette Salido
Nicole Zi Jia Khong
Qiong Liu
Qiong Liu
Rachel Andrea Chea
Hoi Yeung Li
Liang Yang
Liang Yang
Liang Yang
Zhao-Xun Liang
Zhao-Xun Liang
Linghui Xu
Linghui Xu
The MapZ-Mediated Methylation of Chemoreceptors Contributes to Pathogenicity of Pseudomonas aeruginosa
Frontiers in Microbiology
Pseudomonas aeruginosa
chemotaxis
PilZ adaptor
cyclic di-GMP
methyl-accepting chemotaxis protein
methyltransferase cheR1
title The MapZ-Mediated Methylation of Chemoreceptors Contributes to Pathogenicity of Pseudomonas aeruginosa
title_full The MapZ-Mediated Methylation of Chemoreceptors Contributes to Pathogenicity of Pseudomonas aeruginosa
title_fullStr The MapZ-Mediated Methylation of Chemoreceptors Contributes to Pathogenicity of Pseudomonas aeruginosa
title_full_unstemmed The MapZ-Mediated Methylation of Chemoreceptors Contributes to Pathogenicity of Pseudomonas aeruginosa
title_short The MapZ-Mediated Methylation of Chemoreceptors Contributes to Pathogenicity of Pseudomonas aeruginosa
title_sort mapz mediated methylation of chemoreceptors contributes to pathogenicity of pseudomonas aeruginosa
topic Pseudomonas aeruginosa
chemotaxis
PilZ adaptor
cyclic di-GMP
methyl-accepting chemotaxis protein
methyltransferase cheR1
url https://www.frontiersin.org/article/10.3389/fmicb.2019.00067/full
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