The PhzI/PhzR quorum-sensing system is required for pyrrolnitrin and phenazine production, and exhibits cross-regulation with RpoS in Pseudomonas chlororaphis PA23

Selin, Carrie; Fernando, W. G. Dilantha; Kievit, Teresa de

doi:10.1099/mic.0.054254-0

Cited by 57 publications

(75 citation statements)

References 50 publications

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“…However, by extending the growth period from 24 to 48 and 72 h, we found that the production of TDA, as determined by bioactivity and pigment production, was delayed but not completely abolished. Similarly, mutations in QS genes reduced but did not totally suppress the production of biofilm-inhibiting cyclic lipopeptides in Pseudomonas putida (33) or proteases in Pseudomonas chlororaphis (34). Our results show that TDA production in P. gallaeciensis is only modulated by the PgaI-PgaR QS system, and this indicates that QS is just one of several regulatory systems involved.…”

Section: Antagonism Of P Gallaeciensis Qs Mutants In Broth Systemsmentioning

confidence: 53%

“…Therefore, a mutation in the QS system can lead to the complete loss of antibiotic production (31,32) or just cause a reduction in the production of the antagonistic compound (33,34). Berger et al (18) showed that TDA production in P. gallaeciensis is QS regulated.…”

Section: Antagonism Of P Gallaeciensis Qs Mutants In Broth Systemsmentioning

confidence: 99%

“…The production of secondary metabolites, such as antifungal and antibacterial compounds, can be regulated by QS, and this regulation can be absolute (31,32) or just a modulation (33,34). Therefore, a mutation in the QS system can lead to the complete loss of antibiotic production (31,32) or just cause a reduction in the production of the antagonistic compound (33,34).…”

Section: Antagonism Of P Gallaeciensis Qs Mutants In Broth Systemsmentioning

confidence: 99%

“…This is in agreement with previous observations by Berger et al (35), who showed that pgaI and pgaR mutants are able to produce TDA in a minimal medium with phenylalanine as the sole carbon source. In some bacteria, the luxI-luxR QS system forms part of a hierarchically organized network where other regulators are integrated for the control of secondary-metabolite production (34,36), and this type of organization has been suggested previously for TDA production in P. gallaeciensis (35). Our group has recently demonstrated that the expression of the tdaC gene, key in the synthesis of TDA in Ruegeria mobilis, coincides with high levels of the second messenger signal cyclic dimeric guanosinmonophosphate (c-di-GMP), and we have hypothesized that c-di-GMP could be involved in the regulation of TDA synthesis in Roseobacter bacteria (37).…”

Section: Antagonism Of P Gallaeciensis Qs Mutants In Broth Systemsmentioning

confidence: 99%

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Disruption of Cell-to-Cell Signaling Does Not Abolish the Antagonism of Phaeobacter gallaeciensis toward the Fish Pathogen Vibrio anguillarum in Algal Systems

Garcia

D’Alvise

Gram

2013

Appl Environ Microbiol

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Quorum sensing (QS) regulates Phaeobacter gallaeciensis antagonism in broth systems; however, we demonstrate here that QS is not important for antagonism in algal cultures. QS mutants reduced Vibrio anguillarum to the same extent as the wild type. Consequently, a combination of probiotic Phaeobacter and QS inhibitors is a feasible strategy for aquaculture disease control. Bacteria predominantly exist in mixed populations, and the behavior of the complete population is often affected by highly structured and sophisticated ways of communication.Many bacteria secrete small pheromone-like substances that allow the complete population to sense its density and subsequently alter, in a coordinated manner, gene expression. This type of communication between bacteria is known as quorum sensing (QS). QS systems play an important role in the regulation of genes related to virulence and, also, in genes involved in the production of bioactive compounds, such as antibiotics and enzymes (1-4).Roseobacter clade bacteria are some of the most common prokaryotes in oceanic and aquaculture environments (5-7). Some Roseobacter clade species, such as Phaeobacter gallaeciensis, Phaeobacter inhibens, and Ruegeria mobilis, produce a broad-spectrum antibacterial compound known as tropodithietic acid (TDA) (7-9). TDA does not induce resistance in the target organisms (10) and is the key compound for antagonism in laboratory broth cultures (11), in algae and rotifers, and in fish larval systems (12, 13). The ecological role of TDA is not known, but as TDA-producing bacteria can inhibit fish and shellfish pathogens, they have interesting prospects for application as probiotics in aquaculture (13,14).QS compounds of the acylated homoserine lactone (AHL) class are produced by some Roseobacter clade species (15-17), and TDA production is influenced by AHLs in Phaeobacter gallaeciensis. Genes homologous to the classical luxI (pgaI) and luxR (pgaR) genes have been identified, and a 24-h culture supernatant of a pgaI-negative mutant that is unable to produce the AHL compound did not antagonize other bacteria as the wild type did (18). Ruegeria mobilis does not produce AHLs, but in this bacterium, TDA itself can act as an autoinducer, controlling the expression of key genes for TDA production (19).Roseobacter bacteria are frequently associated with algae, both in oceanic waters and aquaculture systems (5, 7). In aquaculture, algae are used as a direct addition to fish larva-rearing tanks and to enrich live prey organisms, such as rotifers and Artemia, with fatty acids. Both algae and live feed have been suggested as vehicles for the introduction of probiotics into rearing systems (20,21), and a strategy of adding Phaeobacter strains to reduce pathogenic Vibrio in live feed and larval cultures has been proposed (12). As P. gallaeciensis antagonism is mainly caused by TDA and since TDA production is regulated by QS, we hypothesized that P. gallaeciensis antagonism in aquaculture settings (e.g., algal cultures) would also be affected by QS and, hence...

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Section: Antagonism Of P Gallaeciensis Qs Mutants In Broth Systemsmentioning

confidence: 53%

Section: Antagonism Of P Gallaeciensis Qs Mutants In Broth Systemsmentioning

confidence: 99%

Section: Antagonism Of P Gallaeciensis Qs Mutants In Broth Systemsmentioning

confidence: 99%

Section: Antagonism Of P Gallaeciensis Qs Mutants In Broth Systemsmentioning

confidence: 99%

See 2 more Smart Citations

Disruption of Cell-to-Cell Signaling Does Not Abolish the Antagonism of Phaeobacter gallaeciensis toward the Fish Pathogen Vibrio anguillarum in Algal Systems

Garcia

D’Alvise

Gram

2013

Appl Environ Microbiol

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“…Previous studies with P. chlororaphis 30-84 established that a hierarchical network of genes regulates the PhzR/PhzI QS system that controls the phenazine biosynthetic operon [16,17]. This includes regulation by the transcriptional regulator Pip, the two-component signal transduction system RpeA/ RpeB, the stationary sigma factor RpoS and the Gac/Rsm system [16][17][18][19][20]. Pip is an important positive regulator of QS in P. chlororaphis 30-84 and PCL1391 [16,18].…”

Section: Introductionmentioning

confidence: 99%

Disruption of MiaA provides insights into the regulation of phenazine biosynthesis under suboptimal growth conditions in Pseudomonas chlororaphis 30-84

Wang

Pierson

et al. 2017

Microbiology

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Many products of secondary metabolism are activated by quorum sensing (QS), yet even at cell densities sufficient for QS, their production may be repressed under suboptimal growth conditions via mechanisms that still require elucidation. For many beneficial plant-associated bacteria, secondary metabolites such as phenazines are important for their competitive survival and plant-protective activities. Previous work established that phenazine biosynthesis in Pseudomonas chlororaphis 30-84 is regulated by the PhzR/PhzI QS system, which in turn is regulated by transcriptional regulator Pip, two-component system RpeA/RpeB and stationary phase/stress sigma factor RpoS. Disruption of MiaA, a tRNA modification enzyme, altered primary metabolism and growth leading to widespread effects on secondary metabolism, including reduced phenazine production and oxidative stress tolerance. Thus, the miaA mutant provided the opportunity to examine the regulation of phenazine production in response to altered metabolism and growth or stress tolerance. Despite the importance of MiaA for translation efficiency, the most significant effect of miaA disruption on phenazine production was the reduction in the transcription of phzR, phzI and pip, whereas neither the transcription nor translation of RpeB, a transcriptional regulator of pip, was affected. Constitutive expression of rpeB or pip in the miaA mutant completely restored phenazine production, but it resulted in further growth impairment. Constitutive expression of RpoS alleviated sensitivity to oxidative stress resulting from RpoS translation inefficiency in the miaA mutant, but it did not restore phenazine production. Our results support the model that cells curtail phenazine biosynthesis under suboptimal growth conditions via RpeB/Pip-mediated regulation of QS.

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Microbiome Genomics and Functional Traits for Agricultural Sustainability

Novinscak

Zboralski

Roquigny

et al. 2020

The Plant Microbiome in Sustainable Agriculture

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The PhzI/PhzR quorum-sensing system is required for pyrrolnitrin and phenazine production, and exhibits cross-regulation with RpoS in Pseudomonas chlororaphis PA23

Cited by 57 publications

References 50 publications

Disruption of Cell-to-Cell Signaling Does Not Abolish the Antagonism of Phaeobacter gallaeciensis toward the Fish Pathogen Vibrio anguillarum in Algal Systems

Disruption of Cell-to-Cell Signaling Does Not Abolish the Antagonism of Phaeobacter gallaeciensis toward the Fish Pathogen Vibrio anguillarum in Algal Systems

Disruption of MiaA provides insights into the regulation of phenazine biosynthesis under suboptimal growth conditions in Pseudomonas chlororaphis 30-84

Microbiome Genomics and Functional Traits for Agricultural Sustainability

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