Surfactant phospholipids act as molecular switches for premature induction of quorum sensing-dependent virulence in Pseudomonas aeruginosa

The virulence behaviors of many Gram-negative bacterial pathogens are governed by quorum-sensing (QS), a hierarchical system of gene regulation that relies on population density by producing and detecting extracellular signaling molecules. Although extensively studied under in vitro conditions, adap...

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Autores principales:	Zhizhou Kuang, Richard C. Bennett, Jingjun Lin, Yonghua Hao, Luchang Zhu, Henry T. Akinbi, Gee W. Lau
Formato:	article
Lenguaje:	EN
Publicado:	Taylor & Francis Group 2020
Materias:	pseudomonas aeruginosa quorum sensing virulence expression elastase b rhamnolipids surfactant phospholipids dipalmitoylphosphatidylcholine Infectious and parasitic diseases RC109-216
Acceso en línea:	https://doaj.org/article/e9f34526d4714c8faae5467e3428f937
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spelling	oai:doaj.org-article:e9f34526d4714c8faae5467e3428f9372021-11-17T14:21:58ZSurfactant phospholipids act as molecular switches for premature induction of quorum sensing-dependent virulence in Pseudomonas aeruginosa2150-55942150-560810.1080/21505594.2020.1809327https://doaj.org/article/e9f34526d4714c8faae5467e3428f9372020-12-01T00:00:00Zhttp://dx.doi.org/10.1080/21505594.2020.1809327https://doaj.org/toc/2150-5594https://doaj.org/toc/2150-5608The virulence behaviors of many Gram-negative bacterial pathogens are governed by quorum-sensing (QS), a hierarchical system of gene regulation that relies on population density by producing and detecting extracellular signaling molecules. Although extensively studied under in vitro conditions, adaptation of QS system to physiologically relevant host environment is not fully understood. In this study, we investigated the influence of lung environment on the regulation of Pseudomonas aeruginosa virulence factors by QS in a mouse model of acute pneumonia. When cultured under laboratory conditions in lysogeny broth, wild-type P. aeruginosa strain PAO1 began to express QS-regulated virulence factors elastase B (LasB) and rhamnolipids (RhlA) during transition from late-exponential into stationary growth phase. In contrast, during acute pneumonia as well as when cultured in mouse bronchial alveolar lavage fluids (BALF), exponential phase PAO1 bacteria at low population density prematurely expressed QS regulatory genes lasI-lasR and rhlI-rhlR and their downstream virulence genes lasB and rhlA. Further analysis indicated that surfactant phospholipids were the primary components within BALF that induced the synthesis of N-(3-oxododecanoyl)-L-homoserine lactone (C12-HSL), which triggered premature expression of LasB and RhlA. Both phenol extraction and phospholipase A2 digestion abolished the ability of mouse BALF to promote LasB and RhlA expression. In contrast, provision of the major surfactant phospholipid dipalmitoylphosphatidylcholine (DPPC) restored the expression of both virulence factors. Collectively, our study demonstrates P. aeruginosa modulates its QS to coordinate the expression of virulence factors during acute pneumonia by recognizing pulmonary surfactant phospholipids.Zhizhou KuangRichard C. BennettJingjun LinYonghua HaoLuchang ZhuHenry T. AkinbiGee W. LauTaylor & Francis Grouparticlepseudomonas aeruginosaquorum sensingvirulence expressionelastase brhamnolipidssurfactant phospholipidsdipalmitoylphosphatidylcholineInfectious and parasitic diseasesRC109-216ENVirulence, Vol 11, Iss 1, Pp 1090-1107 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	pseudomonas aeruginosa quorum sensing virulence expression elastase b rhamnolipids surfactant phospholipids dipalmitoylphosphatidylcholine Infectious and parasitic diseases RC109-216
spellingShingle	pseudomonas aeruginosa quorum sensing virulence expression elastase b rhamnolipids surfactant phospholipids dipalmitoylphosphatidylcholine Infectious and parasitic diseases RC109-216 Zhizhou Kuang Richard C. Bennett Jingjun Lin Yonghua Hao Luchang Zhu Henry T. Akinbi Gee W. Lau Surfactant phospholipids act as molecular switches for premature induction of quorum sensing-dependent virulence in Pseudomonas aeruginosa
description	The virulence behaviors of many Gram-negative bacterial pathogens are governed by quorum-sensing (QS), a hierarchical system of gene regulation that relies on population density by producing and detecting extracellular signaling molecules. Although extensively studied under in vitro conditions, adaptation of QS system to physiologically relevant host environment is not fully understood. In this study, we investigated the influence of lung environment on the regulation of Pseudomonas aeruginosa virulence factors by QS in a mouse model of acute pneumonia. When cultured under laboratory conditions in lysogeny broth, wild-type P. aeruginosa strain PAO1 began to express QS-regulated virulence factors elastase B (LasB) and rhamnolipids (RhlA) during transition from late-exponential into stationary growth phase. In contrast, during acute pneumonia as well as when cultured in mouse bronchial alveolar lavage fluids (BALF), exponential phase PAO1 bacteria at low population density prematurely expressed QS regulatory genes lasI-lasR and rhlI-rhlR and their downstream virulence genes lasB and rhlA. Further analysis indicated that surfactant phospholipids were the primary components within BALF that induced the synthesis of N-(3-oxododecanoyl)-L-homoserine lactone (C12-HSL), which triggered premature expression of LasB and RhlA. Both phenol extraction and phospholipase A2 digestion abolished the ability of mouse BALF to promote LasB and RhlA expression. In contrast, provision of the major surfactant phospholipid dipalmitoylphosphatidylcholine (DPPC) restored the expression of both virulence factors. Collectively, our study demonstrates P. aeruginosa modulates its QS to coordinate the expression of virulence factors during acute pneumonia by recognizing pulmonary surfactant phospholipids.
format	article
author	Zhizhou Kuang Richard C. Bennett Jingjun Lin Yonghua Hao Luchang Zhu Henry T. Akinbi Gee W. Lau
author_facet	Zhizhou Kuang Richard C. Bennett Jingjun Lin Yonghua Hao Luchang Zhu Henry T. Akinbi Gee W. Lau
author_sort	Zhizhou Kuang
title	Surfactant phospholipids act as molecular switches for premature induction of quorum sensing-dependent virulence in Pseudomonas aeruginosa
title_short	Surfactant phospholipids act as molecular switches for premature induction of quorum sensing-dependent virulence in Pseudomonas aeruginosa
title_full	Surfactant phospholipids act as molecular switches for premature induction of quorum sensing-dependent virulence in Pseudomonas aeruginosa
title_fullStr	Surfactant phospholipids act as molecular switches for premature induction of quorum sensing-dependent virulence in Pseudomonas aeruginosa
title_full_unstemmed	Surfactant phospholipids act as molecular switches for premature induction of quorum sensing-dependent virulence in Pseudomonas aeruginosa
title_sort	surfactant phospholipids act as molecular switches for premature induction of quorum sensing-dependent virulence in pseudomonas aeruginosa
publisher	Taylor & Francis Group
publishDate	2020
url	https://doaj.org/article/e9f34526d4714c8faae5467e3428f937
work_keys_str_mv	AT zhizhoukuang surfactantphospholipidsactasmolecularswitchesforprematureinductionofquorumsensingdependentvirulenceinpseudomonasaeruginosa AT richardcbennett surfactantphospholipidsactasmolecularswitchesforprematureinductionofquorumsensingdependentvirulenceinpseudomonasaeruginosa AT jingjunlin surfactantphospholipidsactasmolecularswitchesforprematureinductionofquorumsensingdependentvirulenceinpseudomonasaeruginosa AT yonghuahao surfactantphospholipidsactasmolecularswitchesforprematureinductionofquorumsensingdependentvirulenceinpseudomonasaeruginosa AT luchangzhu surfactantphospholipidsactasmolecularswitchesforprematureinductionofquorumsensingdependentvirulenceinpseudomonasaeruginosa AT henrytakinbi surfactantphospholipidsactasmolecularswitchesforprematureinductionofquorumsensingdependentvirulenceinpseudomonasaeruginosa AT geewlau surfactantphospholipidsactasmolecularswitchesforprematureinductionofquorumsensingdependentvirulenceinpseudomonasaeruginosa
_version_	1718425518627356672

Surfactant phospholipids act as molecular switches for premature induction of quorum sensing-dependent virulence in Pseudomonas aeruginosa

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