Pseudomonas aeruginosa Quorum-Sensing and Type VI Secretion System Can Direct Interspecific Coexistence During Evolution

It is reported that a wide range of bacterial infections are polymicrobial, and the members in a local microcommunity can influence the growth of neighbors through physical and chemical interactions. Pseudomonas aeruginosa is an important opportunistic pathogen that normally causes a variety of acut...

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Main Authors: Kelei Zhao, Lianming Du, Jiafu Lin, Yang Yuan, Xiwei Wang, Bisong Yue, Xinrong Wang, Yidong Guo, Yiwen Chu, Yingshun Zhou
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-10-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2018.02287/full
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spelling doaj-87ded4abee2a4f38bcb206994b235c2b2020-11-25T02:34:43ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-10-01910.3389/fmicb.2018.02287414124Pseudomonas aeruginosa Quorum-Sensing and Type VI Secretion System Can Direct Interspecific Coexistence During EvolutionKelei Zhao0Lianming Du1Jiafu Lin2Yang Yuan3Xiwei Wang4Bisong Yue5Xinrong Wang6Yidong Guo7Yiwen Chu8Yingshun Zhou9Antibiotics Research and Re-evaluation Key Laboratory of Sichuan Province, Sichuan Industrial Institute of Antibiotics, Chengdu University, Chengdu, ChinaInstitute for Advanced Study, Chengdu University, Chengdu, ChinaAntibiotics Research and Re-evaluation Key Laboratory of Sichuan Province, Sichuan Industrial Institute of Antibiotics, Chengdu University, Chengdu, ChinaAntibiotics Research and Re-evaluation Key Laboratory of Sichuan Province, Sichuan Industrial Institute of Antibiotics, Chengdu University, Chengdu, ChinaAntibiotics Research and Re-evaluation Key Laboratory of Sichuan Province, Sichuan Industrial Institute of Antibiotics, Chengdu University, Chengdu, ChinaKey Laboratory of Bio-Resources and Eco-Environment (Ministry of Education), College of Life Sciences, Sichuan University, Chengdu, ChinaAntibiotics Research and Re-evaluation Key Laboratory of Sichuan Province, Sichuan Industrial Institute of Antibiotics, Chengdu University, Chengdu, ChinaAntibiotics Research and Re-evaluation Key Laboratory of Sichuan Province, Sichuan Industrial Institute of Antibiotics, Chengdu University, Chengdu, ChinaAntibiotics Research and Re-evaluation Key Laboratory of Sichuan Province, Sichuan Industrial Institute of Antibiotics, Chengdu University, Chengdu, ChinaDepartment of Pathogenic Biology, College of Preclinical Medicine, Southwest Medical University, Luzhou, ChinaIt is reported that a wide range of bacterial infections are polymicrobial, and the members in a local microcommunity can influence the growth of neighbors through physical and chemical interactions. Pseudomonas aeruginosa is an important opportunistic pathogen that normally causes a variety of acute and chronic infections, and clinical evidences suggest that P. aeruginosa can be frequently coisolated with other pathogens from the patients with chronic infections. However, the interspecific interaction and the coexisting mechanism of P. aeruginosa with coinfecting bacterial species during evolution still remain largely unclear. In this study, the relationships of P. aeruginosa with other Gram-positive (Staphylococcus aureus) and Gram-negative (Klebsiella pneumoniae) are investigated by using a series of on-plate proximity assay, in vitro coevolution assay, and RNA-sequencing. We find that although the development of a quorum-sensing system contributes P. aeruginosa a significant growth advantage to compete with S. aureus and K. pneumoniae, the quorum-sensing regulation of P. aeruginosa will be decreased during evolution and thus provides a basis for the formation of interspecific coexistence. The results of comparative transcriptomic analyses suggest that the persistent survival of S. aureus in the microcommunity has no significant effect on the intracellular transcriptional pattern of P. aeruginosa, while a more detailed competition happens between P. aeruginosa and K. pneumoniae. Specifically, the population of P. aeruginosa with decreased quorum-sensing regulation can still restrict the proportion increase of K. pneumoniae by enhancing the type VI secretion system-elicited cell aggressivity during further coevolution. These findings provide a general explanation for the formation of a dynamic stable microcommunity consisting of more than two bacterial species, and may contribute to the development of population biology and clinical therapy.https://www.frontiersin.org/article/10.3389/fmicb.2018.02287/fullPseudomonas aeruginosaquorum-sensingT6SSevolutioncoexistencemicrocommunity
collection DOAJ
language English
format Article
sources DOAJ
author Kelei Zhao
Lianming Du
Jiafu Lin
Yang Yuan
Xiwei Wang
Bisong Yue
Xinrong Wang
Yidong Guo
Yiwen Chu
Yingshun Zhou
spellingShingle Kelei Zhao
Lianming Du
Jiafu Lin
Yang Yuan
Xiwei Wang
Bisong Yue
Xinrong Wang
Yidong Guo
Yiwen Chu
Yingshun Zhou
Pseudomonas aeruginosa Quorum-Sensing and Type VI Secretion System Can Direct Interspecific Coexistence During Evolution
Frontiers in Microbiology
Pseudomonas aeruginosa
quorum-sensing
T6SS
evolution
coexistence
microcommunity
author_facet Kelei Zhao
Lianming Du
Jiafu Lin
Yang Yuan
Xiwei Wang
Bisong Yue
Xinrong Wang
Yidong Guo
Yiwen Chu
Yingshun Zhou
author_sort Kelei Zhao
title Pseudomonas aeruginosa Quorum-Sensing and Type VI Secretion System Can Direct Interspecific Coexistence During Evolution
title_short Pseudomonas aeruginosa Quorum-Sensing and Type VI Secretion System Can Direct Interspecific Coexistence During Evolution
title_full Pseudomonas aeruginosa Quorum-Sensing and Type VI Secretion System Can Direct Interspecific Coexistence During Evolution
title_fullStr Pseudomonas aeruginosa Quorum-Sensing and Type VI Secretion System Can Direct Interspecific Coexistence During Evolution
title_full_unstemmed Pseudomonas aeruginosa Quorum-Sensing and Type VI Secretion System Can Direct Interspecific Coexistence During Evolution
title_sort pseudomonas aeruginosa quorum-sensing and type vi secretion system can direct interspecific coexistence during evolution
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2018-10-01
description It is reported that a wide range of bacterial infections are polymicrobial, and the members in a local microcommunity can influence the growth of neighbors through physical and chemical interactions. Pseudomonas aeruginosa is an important opportunistic pathogen that normally causes a variety of acute and chronic infections, and clinical evidences suggest that P. aeruginosa can be frequently coisolated with other pathogens from the patients with chronic infections. However, the interspecific interaction and the coexisting mechanism of P. aeruginosa with coinfecting bacterial species during evolution still remain largely unclear. In this study, the relationships of P. aeruginosa with other Gram-positive (Staphylococcus aureus) and Gram-negative (Klebsiella pneumoniae) are investigated by using a series of on-plate proximity assay, in vitro coevolution assay, and RNA-sequencing. We find that although the development of a quorum-sensing system contributes P. aeruginosa a significant growth advantage to compete with S. aureus and K. pneumoniae, the quorum-sensing regulation of P. aeruginosa will be decreased during evolution and thus provides a basis for the formation of interspecific coexistence. The results of comparative transcriptomic analyses suggest that the persistent survival of S. aureus in the microcommunity has no significant effect on the intracellular transcriptional pattern of P. aeruginosa, while a more detailed competition happens between P. aeruginosa and K. pneumoniae. Specifically, the population of P. aeruginosa with decreased quorum-sensing regulation can still restrict the proportion increase of K. pneumoniae by enhancing the type VI secretion system-elicited cell aggressivity during further coevolution. These findings provide a general explanation for the formation of a dynamic stable microcommunity consisting of more than two bacterial species, and may contribute to the development of population biology and clinical therapy.
topic Pseudomonas aeruginosa
quorum-sensing
T6SS
evolution
coexistence
microcommunity
url https://www.frontiersin.org/article/10.3389/fmicb.2018.02287/full
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