Putative RNA Ligase RtcB Affects the Switch between T6SS and T3SS in <i>Pseudomonas aeruginosa</i>

The opportunistic pathogen <i>Pseudomonas aeruginosa</i> is a significant cause of infection in immunocompromised individuals, cystic fibrosis patients, and burn victims. To benefit its survival, the bacterium adapt to either a motile or sessile lifestyle when infecting the host. The mot...

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Autores principales:	Maryam Dadashi, Lin Chen, Ahmad Nasimian, Saeid Ghavami, Kangmin Duan
Formato:	article
Lenguaje:	EN
Publicado:	MDPI AG 2021
Materias:	virulence factors T6SS T3SS c-di-GMP <i>P. aeruginosa</i> microbial competition Biology (General) QH301-705.5 Chemistry QD1-999
Acceso en línea:	https://doaj.org/article/887bf12f8dc3426a8522581790966cdf
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spelling	oai:doaj.org-article:887bf12f8dc3426a8522581790966cdf2021-11-25T17:57:50ZPutative RNA Ligase RtcB Affects the Switch between T6SS and T3SS in <i>Pseudomonas aeruginosa</i>10.3390/ijms2222125611422-00671661-6596https://doaj.org/article/887bf12f8dc3426a8522581790966cdf2021-11-01T00:00:00Zhttps://www.mdpi.com/1422-0067/22/22/12561https://doaj.org/toc/1661-6596https://doaj.org/toc/1422-0067The opportunistic pathogen <i>Pseudomonas aeruginosa</i> is a significant cause of infection in immunocompromised individuals, cystic fibrosis patients, and burn victims. To benefit its survival, the bacterium adapt to either a motile or sessile lifestyle when infecting the host. The motile bacterium has an often activated type III secretion system (T3SS), which is virulent to the host, whereas the sessile bacterium harbors an active T6SS and lives in biofilms. Regulatory pathways involving Gac-Rsm or secondary messengers such as c-di-GMP determine which lifestyle is favorable for <i>P. aeruginosa</i>. Here, we introduce the RNA binding protein RtcB as a modulator of the switch between motile and sessile bacterial lifestyles. Using the wild-type <i>P. aeruginosa</i> PAO1, and a <i>retS</i> mutant PAO1(∆<i>retS</i>) in which T3SS is repressed and T6SS active, we show that deleting <i>rtcB</i> led to simultaneous expression of T3SS and T6SS in both PAO1(∆<i>rtcB</i>) and PAO1(∆<i>rtcB</i>∆<i>retS</i>). The deletion of <i>rtcB</i> also increased biofilm formation in PAO1(∆<i>rtcB</i>) and restored the motility of PAO1(∆<i>rtcB</i>∆<i>retS</i>). RNA-sequencing data suggested RtcB as a global modulator affecting multiple virulence factors, including bacterial secretion systems. Competitive killing and infection assays showed that the three T6SS systems (H1, H2, and H3) in PAO1(∆<i>rtcB</i>) were activated into a functional syringe, and could compete with <i>Escherichia coli</i> and effectively infect lettuce. Western blotting and RT-PCR results showed that RtcB probably exerted its function through RsmA in PAO1(∆<i>rtcB</i>∆<i>retS</i>). Quantification of c-di-GMP showed an elevated intracellular levels in PAO1(∆<i>rtcB</i>), which likely drove the switch between T6SS and T3SS, and contributed to the altered phenotypes and characteristics observed. Our data demonstrate a pivotal role of RtcB in the virulence of <i>P. aeruginosa</i> by controlling multiple virulence determinants, such as biofilm formation, motility, pyocyanin production, T3SS, and T6SS secretion systems towards eukaryotic and prokaryotic cells. These findings suggest RtcB as a potential target for controlling <i>P. aeruginosa</i> colonization, establishment, and pathogenicity.Maryam DadashiLin ChenAhmad NasimianSaeid GhavamiKangmin DuanMDPI AGarticlevirulence factorsT6SST3SSc-di-GMP<i>P. aeruginosa</i>microbial competitionBiology (General)QH301-705.5ChemistryQD1-999ENInternational Journal of Molecular Sciences, Vol 22, Iss 12561, p 12561 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	virulence factors T6SS T3SS c-di-GMP <i>P. aeruginosa</i> microbial competition Biology (General) QH301-705.5 Chemistry QD1-999
spellingShingle	virulence factors T6SS T3SS c-di-GMP <i>P. aeruginosa</i> microbial competition Biology (General) QH301-705.5 Chemistry QD1-999 Maryam Dadashi Lin Chen Ahmad Nasimian Saeid Ghavami Kangmin Duan Putative RNA Ligase RtcB Affects the Switch between T6SS and T3SS in <i>Pseudomonas aeruginosa</i>
description	The opportunistic pathogen <i>Pseudomonas aeruginosa</i> is a significant cause of infection in immunocompromised individuals, cystic fibrosis patients, and burn victims. To benefit its survival, the bacterium adapt to either a motile or sessile lifestyle when infecting the host. The motile bacterium has an often activated type III secretion system (T3SS), which is virulent to the host, whereas the sessile bacterium harbors an active T6SS and lives in biofilms. Regulatory pathways involving Gac-Rsm or secondary messengers such as c-di-GMP determine which lifestyle is favorable for <i>P. aeruginosa</i>. Here, we introduce the RNA binding protein RtcB as a modulator of the switch between motile and sessile bacterial lifestyles. Using the wild-type <i>P. aeruginosa</i> PAO1, and a <i>retS</i> mutant PAO1(∆<i>retS</i>) in which T3SS is repressed and T6SS active, we show that deleting <i>rtcB</i> led to simultaneous expression of T3SS and T6SS in both PAO1(∆<i>rtcB</i>) and PAO1(∆<i>rtcB</i>∆<i>retS</i>). The deletion of <i>rtcB</i> also increased biofilm formation in PAO1(∆<i>rtcB</i>) and restored the motility of PAO1(∆<i>rtcB</i>∆<i>retS</i>). RNA-sequencing data suggested RtcB as a global modulator affecting multiple virulence factors, including bacterial secretion systems. Competitive killing and infection assays showed that the three T6SS systems (H1, H2, and H3) in PAO1(∆<i>rtcB</i>) were activated into a functional syringe, and could compete with <i>Escherichia coli</i> and effectively infect lettuce. Western blotting and RT-PCR results showed that RtcB probably exerted its function through RsmA in PAO1(∆<i>rtcB</i>∆<i>retS</i>). Quantification of c-di-GMP showed an elevated intracellular levels in PAO1(∆<i>rtcB</i>), which likely drove the switch between T6SS and T3SS, and contributed to the altered phenotypes and characteristics observed. Our data demonstrate a pivotal role of RtcB in the virulence of <i>P. aeruginosa</i> by controlling multiple virulence determinants, such as biofilm formation, motility, pyocyanin production, T3SS, and T6SS secretion systems towards eukaryotic and prokaryotic cells. These findings suggest RtcB as a potential target for controlling <i>P. aeruginosa</i> colonization, establishment, and pathogenicity.
format	article
author	Maryam Dadashi Lin Chen Ahmad Nasimian Saeid Ghavami Kangmin Duan
author_facet	Maryam Dadashi Lin Chen Ahmad Nasimian Saeid Ghavami Kangmin Duan
author_sort	Maryam Dadashi
title	Putative RNA Ligase RtcB Affects the Switch between T6SS and T3SS in <i>Pseudomonas aeruginosa</i>
title_short	Putative RNA Ligase RtcB Affects the Switch between T6SS and T3SS in <i>Pseudomonas aeruginosa</i>
title_full	Putative RNA Ligase RtcB Affects the Switch between T6SS and T3SS in <i>Pseudomonas aeruginosa</i>
title_fullStr	Putative RNA Ligase RtcB Affects the Switch between T6SS and T3SS in <i>Pseudomonas aeruginosa</i>
title_full_unstemmed	Putative RNA Ligase RtcB Affects the Switch between T6SS and T3SS in <i>Pseudomonas aeruginosa</i>
title_sort	putative rna ligase rtcb affects the switch between t6ss and t3ss in <i>pseudomonas aeruginosa</i>
publisher	MDPI AG
publishDate	2021
url	https://doaj.org/article/887bf12f8dc3426a8522581790966cdf
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Putative RNA Ligase RtcB Affects the Switch between T6SS and T3SS in <i>Pseudomonas aeruginosa</i>

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