Quorum sensing restrains growth and is rapidly inactivated during domestication of <scp><i>S</i></scp><i>inorhizobium meliloti</i>

Charoenpanich, Pornsri; Soto, Marı́a José; Becker, Anke; McIntosh, Matthew

doi:10.1111/1758-2229.12262

Cited by 12 publications

(21 citation statements)

References 48 publications

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“…This is plausible, since the AHL receptor ExpR of S . meliloti was also found to restrain growth specifically in the presence of AHLs and under nutrient limiting conditions (Charoenpanich et al ., ). We speculate that QS in R .…”

Section: Resultsmentioning

confidence: 97%

“…These results imply that QS regulation somehow controls growth, as is the case with QS in S . meliloti (Charoenpanich et al ., ). Like all α‐proteobacteria, S .…”

Section: Discussionmentioning

confidence: 97%

“…The observation that cells grew very poorly in the absence of AHLs on one hand, and not at all upon cerR overexpression on the other is extremely interesting and suggests that regulation by the Cer QS extends to the control of growth and adaption to stationary phase. This is plausible, since the AHL receptor ExpR of S. meliloti was also found to restrain growth specifically in the presence of AHLs and under nutrient limiting conditions (Charoenpanich et al, 2015). We speculate that QS in R. sphaeroides and in S. meliloti provides a means of adapting growth behaviour in a manner analogous to the sigma factor SigB, which promotes dispersal and restrains growth within the B. subtilis mature biofilm (Bartolini et al, 2019).…”

Section: Integration Of Quorum Sensing and Growth Behaviourmentioning

confidence: 89%

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Adaptation of the Alphaproteobacterium Rhodobacter sphaeroides to stationary phase

McIntosh

Eisenhardt

Remes

et al. 2019

Environmental Microbiology

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Summary Exhaustion of nutritional resources stimulates bacterial populations to adapt their growth behaviour. General mechanisms are known to facilitate this adaptation by sensing the environmental change and coordinating gene expression. However, the existence of such mechanisms among the Alphaproteobacteria remains unclear. This study focusses on global changes in transcript levels during growth under carbon‐limiting conditions in a model Alphaproteobacterium, Rhodobacter sphaeroides, a metabolically diverse organism capable of multiple modes of growth including aerobic and anaerobic respiration, anaerobic anoxygenic photosynthesis and fermentation. We identified genes that showed changed transcript levels independently of oxygen levels during the adaptation to stationary phase. We selected a subset of these genes and subjected them to mutational analysis, including genes predicted to be involved in manganese uptake, polyhydroxybutyrate production and quorum sensing and an alternative sigma factor. Although these genes have not been previously associated with the adaptation to stationary phase, we found that all were important to varying degrees. We conclude that while R. sphaeroides appears to lack a rpoS‐like master regulator of stationary phase adaptation, this adaptation is nonetheless enabled through the impact of multiple genes, each responding to environmental conditions and contributing to the adaptation to stationary phase.

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Section: Resultsmentioning

confidence: 97%

“…These results imply that QS regulation somehow controls growth, as is the case with QS in S . meliloti (Charoenpanich et al ., ). Like all α‐proteobacteria, S .…”

Section: Discussionmentioning

confidence: 97%

Section: Integration Of Quorum Sensing and Growth Behaviourmentioning

confidence: 89%

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Adaptation of the Alphaproteobacterium Rhodobacter sphaeroides to stationary phase

McIntosh

Eisenhardt

Remes

et al. 2019

Environmental Microbiology

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“…ExpR, whose activity depends on N-acyl-homoserine lactones (AHLs), regulates expression of nearly 9% of S. meliloti genes, including those important for quorum sensing, motility, and EPS biosynthesis (114)(115)(116). ExpR ϩ strains are difficult to cultivate and manipulate in the lab because of their extremely mucoid colonial morphology and negative selection acting against a functional expR gene (117). Global analyses of ExpR function suggest that ExpR does not regulate SyrM, NodD3, or SyrA expression (70,115,116).…”

Section: Discussionmentioning

confidence: 99%

The Sinorhizobium meliloti SyrM Regulon: Effects on Global Gene Expression Are Mediated by syrA and nodD3

Barnett

Long

2015

J Bacteriol

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In Sinorhizobium meliloti, three NodD transcriptional regulators activate bacterial nodulation (nod) gene expression. NodD1 and NodD2 require plant compounds to activate nod genes. The NodD3 protein does not require exogenous compounds to activate nod gene expression; instead, another transcriptional regulator, SyrM, activates nodD3 expression. In addition, NodD3 can activate syrM expression. SyrM also activates expression of another gene, syrA, which when overexpressed causes a dramatic increase in exopolysaccharide production. In a previous study, we identified more than 200 genes with altered expression in a strain overexpressing nodD3. In this work, we define the transcriptomes of strains overexpressing syrM or syrA. The syrM, nodD3, and syrA overexpression transcriptomes share similar gene expression changes; analyses imply that nodD3 and syrA are the only targets directly activated by SyrM. We propose that most of the gene expression changes observed when nodD3 is overexpressed are due to NodD3 activation of syrM expression, which in turn stimulates SyrM activation of syrA expression. The subsequent increase in SyrA abundance results in broad changes in gene expression, most likely mediated by the ChvI-ExoS-ExoR regulatory circuit. IMPORTANCESymbioses with bacteria are prevalent across the animal and plant kingdoms. Our system of study, the rhizobium-legume symbiosis (Sinorhizobium meliloti and Medicago spp.), involves specific host-microbe signaling, differentiation in both partners, and metabolic exchange of bacterial fixed nitrogen for host photosynthate. During this complex developmental process, both bacteria and plants undergo profound changes in gene expression. The S. meliloti SyrM-NodD3-SyrA and ChvI-ExoS-ExoR regulatory circuits affect gene expression and are important for optimal symbiosis. In this study, we defined the transcriptomes of S. meliloti overexpressing SyrM or SyrA. In addition to identifying new targets of the SyrM-NodD3-SyrA regulatory circuit, our work further suggests how it is linked to the ChvI-ExoS-ExoR regulatory circuit. The symbiotic soil alphaproteobacterium Sinorhizobium meliloti forms nitrogen-fixing nodules on the roots of leguminous plants such as Medicago sativa (alfalfa) and Medicago truncatula (barrel medic). The earliest stages of the symbiosis involve an exchange of molecular signals: plant roots exude compounds that induce transcription of bacterial nod genes, which encode enzymes that synthesize lipochitooligosaccharide Nod factors (NF) (1, 2). These bacterial NF trigger early plant responses such as root hair curling, calcium spiking, and root cortical cell divisions to form the nodule organ (2). Bacteria trapped in curled root hairs penetrate the root hair through an infection thread (IT), an ingrowth of plant cell membrane and wall (3). As the IT elongates into the root, the bacteria at the tip are actively dividing.Bacterial polysaccharides, such as cyclic ␤-glucans and exopolysaccharide I (EPS-I; also known as succinoglycan), are essential for bacte...

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“…The master regulator TraR thus appears the preferential target for reducing the cost associated with the QS-activity, but one could not exclude that mutations in other loci, such as traI coding for QS-signal production, may occur. In Sinorhizobium(Ensifer) meliloti and Pseudomonas aeruginosa , mutations in the genes coding the master QS-regulators ExpR and LasR are also preferentially selected under costly QS-conditions103536.…”

Section: Discussionmentioning

confidence: 99%

Quorum-quenching limits quorum-sensing exploitation by signal-negative invaders

Tannières

Lang

Barnier

et al. 2017

Sci Rep

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Some bacteria produce and perceive quorum-sensing (QS) signals that coordinate several behaviours, including the costly processes that are exoenzyme production and plasmid transfer. In the case of plasmid transfer, the emergence of QS signal-altered invaders and their policing are poorly documented. In Agrobacterium tumefaciens, the virulence Ti-plasmid encodes both synthesis and sensing of QS-signals, which promote its transfer from a donor to a recipient cell. Here, we reported that QS-altered A. tumefaciens mutants arose during experimental evolution. All showed improved growth compared to their ancestor. Genome sequencing revealed that, though some had lost the Ti-plasmid, most were defective for QS-signal synthesis and Ti-plasmid conjugation (traR mutations) and one exhibited a QS-signal exploitation behaviour, using signal produced by other cells to enhance its own Ti-plasmid transfer. We explored mechanisms that can limit this QS-hijacking. We showed that the A. tumefaciens capacity to inactivate QS-signals by expressing QS-degrading enzyme could attenuate dissemination of the QS signal-negative Ti-plasmids. This work shows that enzymatic QS-disruption whether encoded by the QS-producing Ti-plasmid itself, by a companion plasmid in the same donor cells, or by one in the recipient cells, in all cases can serve as a mechanism for controlling QS exploitation by QS signal-negative mutants.

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Quorum sensing restrains growth and is rapidly inactivated during domestication of Sinorhizobium meliloti

Cited by 12 publications

References 48 publications

Adaptation of the Alphaproteobacterium Rhodobacter sphaeroides to stationary phase

Adaptation of the Alphaproteobacterium Rhodobacter sphaeroides to stationary phase

The Sinorhizobium meliloti SyrM Regulon: Effects on Global Gene Expression Are Mediated by syrA and nodD3

Quorum-quenching limits quorum-sensing exploitation by signal-negative invaders

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