Investigation of the quorum-sensing regulon of the biocontrol bacterium Pseudomonas chlororaphis strain PA23

Shah, Nidhi; Gislason, April S.; Becker, Michael G.; Belmonte, Mark F.; Fernando, W. G. Dilantha; Kievit, Teresa R. de

doi:10.1371/journal.pone.0226232

Cited by 18 publications

(12 citation statements)

References 61 publications

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“…However, specific AI-2-related responses can be found in the expression of genes involved in the composition of cellular membranes and elements associated with various processes, such as bacterial motility, DNA repair, inorganic nutrient metabolism, and carbohydrate degradation. Interestingly, similar scenarios have also been observed during the QS response in additional bacterial species [26][27][28][29][30][31][32][33][34][35][36][37][38][39][40][41][42][43][44][45].…”

Section: Discussionsupporting

confidence: 68%

The Quorum Sensing Auto-Inducer 2 (AI-2) Stimulates Nitrogen Fixation and Favors Ethanol Production over Biomass Accumulation in Zymomonas mobilis

Alencar

Silva

Boas

et al. 2021

IJMS

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Autoinducer 2 (or AI-2) is one of the molecules used by bacteria to trigger the Quorum Sensing (QS) response, which activates expression of genes involved in a series of alternative mechanisms, when cells reach high population densities (including bioluminescence, motility, biofilm formation, stress resistance, and production of public goods, or pathogenicity factors, among others). Contrary to most autoinducers, AI-2 can induce QS responses in both Gram-negative and Gram-positive bacteria, and has been suggested to constitute a trans-specific system of bacterial communication, capable of affecting even bacteria that cannot produce this autoinducer. In this work, we demonstrate that the ethanologenic Gram-negative bacterium Zymomonas mobilis (a non-AI-2 producer) responds to exogenous AI-2 by modulating expression of genes involved in mechanisms typically associated with QS in other bacteria, such as motility, DNA repair, and nitrogen fixation. Interestingly, the metabolism of AI-2-induced Z. mobilis cells seems to favor ethanol production over biomass accumulation, probably as an adaptation to the high-energy demand of N2 fixation. This opens the possibility of employing AI-2 during the industrial production of second-generation ethanol, as a way to boost N2 fixation by these bacteria, which could reduce costs associated with the use of nitrogen-based fertilizers, without compromising ethanol production in industrial plants.

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Section: Discussionsupporting

confidence: 68%

The Quorum Sensing Auto-Inducer 2 (AI-2) Stimulates Nitrogen Fixation and Favors Ethanol Production over Biomass Accumulation in Zymomonas mobilis

Alencar

Silva

Boas

et al. 2021

IJMS

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“…In agreement with our data, it has been described that mutation of QS systems leads to increased siderophores in Burkholderia ambifaria , Pseudomonas chlororaphis , and Vibrio vulnificus . 14,15,17 To understand how the CviIR QS system controls siderophore levels in C. violaceum , we identified the entire repertoire of CviR and CviI-regulated genes (Figure 7) and checked whether their regulation was cell-density dependent (Figure 8). Surprisingly, we found that CviR regulates CviI-dependent and CviI-independent regulons, suggesting that CviR can act regardless of its canonical CviI autoinducers, which in C. violaceum ATCC 12472 are several long-chain AHLs.…”

Section: Discussionmentioning

confidence: 99%

“…13 Considering that siderophores are known as public goods, it is not surprising that the QS systems of some bacteria regulate siderophore production. 14,15,16,17…”

Section: Introductionmentioning

confidence: 99%

A complex regulatory cascade involving quorum sensing regulates siderophore-mediated iron homeostasis inChromobacterium violaceum

Batista,

de Lima,

Picinato

et al. 2023

Preprint

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Iron is a transition metal used as a cofactor in many biochemical reactions. In bacteria, iron homeostasis involves Fur-mediated de-repression of iron uptake systems, such as the iron-chelating compounds siderophores. In this work, we identified and characterized novel regulatory systems that control siderophores in the environmental opportunistic pathogenChromobacterium violaceum. Screening of a 10,000-transposon mutant library for siderophore halos on PSA-CAS plates identified seven possible regulatory systems involved in siderophore-mediated iron homeostasis inC. violaceum. Further characterization revealed a regulatory cascade that controls siderophores involving the transcription factor VitR acting upstream of the quorum sensing (QS) system CviIR. Mutation of the regulator VitR led to an increase in siderophore halos, and a decrease in biofilm, violacein, and protease production. We determined that these effects occurred due to VitR-dependent de-repression ofvioS. Increased VioS leads to direct inhibition of the CviR regulator by protein-protein interaction. Indeed, insertion mutations incviRand null mutation ofcviIandcviRled to an increase of siderophore halos. RNA-seq of thecviIandcviRmutants revealed that CviR regulates CviI-dependent and CviI-independent regulons. Classical QS-dependent processes (violacein, proteases, and antibiotics) were activated at high cell density by both CviI and CviR. However, genes related to iron homeostasis and many other processes were regulated by CviR but not CviI, suggesting that CviR acts without its canonical CviI autoinducer. Our data revealed a complex regulatory cascade involving QS that controls siderophore-mediated iron homeostasis inC. violaceum.ImportanceThe iron-chelating compounds siderophores play a major role in bacterial iron acquisition. Here, we employed a genetic screen to identify novel siderophore regulatory systems inChromobacterium violaceum, an opportunistic human pathogen. Many mutants with increased siderophore halos had transposon insertions in genes encoding transcription factors, including a novel regulator called VitR, and CviR, the regulator of the quorum sensing (QS) system CviIR. We found that VitR is upstream in the pathway and acts as a dedicated repressor ofvioS, which encodes a direct CviR-inhibitory protein. Indeed, all QS-related phenotypes of avitRmutant were rescued in avitRvioSmutant. At high cell density, CviIR activated classical QS-dependent processes (violacein, proteases, and antibiotics production). However, genes related to iron homeostasis and type-III and type-VI secretion systems were regulated by CviR in a CviI- or cell density-independent manner. Our data unveil a complex regulatory cascade integrating QS and siderophores inC. violaceum.

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“…Iron homeostasis can be integrated into quorum-sensing (QS) circuits, a cell-cell communication process in which cells produce, detect, and respond to signaling molecules called autoinducers ( 13 ). Considering that siderophores are known as public goods, it is not surprising that the QS systems of some bacteria regulate siderophore production ( 14 – 17 ).…”

Section: Introductionmentioning

confidence: 99%

A quorum-sensing regulatory cascade for siderophore-mediated iron homeostasis in Chromobacterium violaceum

Batista,

de Lima,

Picinato

et al. 2024

mSystems

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Iron is a transition metal used as a cofactor in many biochemical reactions. In bacteria, iron homeostasis involves Fur-mediated de-repression of iron uptake systems, such as the iron-chelating compounds siderophores. In this work, we identified and characterized novel regulatory systems that control siderophores in the environmental opportunistic pathogen Chromobacterium violaceum . Screening of a 10,000-transposon mutant library for siderophore halos identified seven possible regulatory systems involved in siderophore-mediated iron homeostasis in C. violaceum . Further characterization revealed a regulatory cascade that controls siderophores involving the transcription factor VitR acting upstream of the quorum-sensing (QS) system CviIR. Mutation of the regulator VitR led to an increase in siderophore halos, and a decrease in biofilm, violacein, and protease production. We determined that these effects occurred due to VitR-dependent de-repression of vioS . Increased VioS leads to direct inhibition of the CviR regulator by protein-protein interaction. Indeed, insertion mutations in cviR and null mutations of cviI and cviR led to an increase of siderophore halos. RNA-seq of the cviI and cviR mutants revealed that CviR regulates CviI-dependent and CviI-independent regulons. Classical QS-dependent processes (violacein, proteases, and antibiotics) were activated at high cell density by both CviI and CviR. However, genes related to iron homeostasis and many other processes were regulated by CviR but not CviI, suggesting that CviR acts without its canonical CviI autoinducer. Our data revealed a complex regulatory cascade involving QS that controls siderophore-mediated iron homeostasis in C. violaceum . IMPORTANCE The iron-chelating compounds siderophores play a major role in bacterial iron acquisition. Here, we employed a genetic screen to identify novel siderophore regulatory systems in Chromobacterium violaceum , an opportunistic human pathogen. Many mutants with increased siderophore halos had transposon insertions in genes encoding transcription factors, including a novel regulator called VitR, and CviR, the regulator of the quorum-sensing (QS) system CviIR. We found that VitR is upstream in the pathway and acts as a dedicated repressor of vioS , which encodes a direct CviR-inhibitory protein. Indeed, all QS-related phenotypes of a vitR mutant were rescued in a vitRvioS mutant. At high cell density, CviIR activated classical QS-dependent processes (violacein, proteases, and antibiotics production). However, genes related to iron homeostasis and type-III and type-VI secretion systems were regulated by CviR in a CviI- or cell density-independent manner. Our data unveil a complex regulatory cascade integrating QS and siderophores in C. violaceum .

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Investigation of the quorum-sensing regulon of the biocontrol bacterium Pseudomonas chlororaphis strain PA23

Cited by 18 publications

References 61 publications

The Quorum Sensing Auto-Inducer 2 (AI-2) Stimulates Nitrogen Fixation and Favors Ethanol Production over Biomass Accumulation in Zymomonas mobilis

The Quorum Sensing Auto-Inducer 2 (AI-2) Stimulates Nitrogen Fixation and Favors Ethanol Production over Biomass Accumulation in Zymomonas mobilis

A complex regulatory cascade involving quorum sensing regulates siderophore-mediated iron homeostasis inChromobacterium violaceum

A quorum-sensing regulatory cascade for siderophore-mediated iron homeostasis in Chromobacterium violaceum

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