Clarifying intercellular signalling in yeast: Saccharomyces cerevisiae does not undergo a quorum sensing-dependent switch to filamentous growth

Saccharomyces cerevisiae can alter its morphology to a filamentous form associated with unipolar budding in response to environmental stressors. Induction of filamentous growth is suggested under nitrogen deficiency in response to alcoholic signalling molecules through a quorum sensing mechanism. To investigate this claim, we analysed the budding pattern of S. cerevisiae cells over time under low nitrogen while concurrently measuring cell density and extracellular metabolite concentration. We found that the proportion of cells displaying unipolar budding increased between local cell densities of 4.8x106 and 5.3x107 cells/ml within 10 to 20 hours of growth. However, the observed increase in unipolar budding could not be reproduced when cells were prepared at the critical cell density and in conditioned media. Removing the nutrient restriction by growth in high nitrogen conditions also resulted in an increase in unipolar budding between local cell densities of 5.2x106 and 8.2x107 cells/ml within 10 to 20 hours of growth, but there were differences in metabolite concentration compared to the low nitrogen conditions. This suggests that neither cell density, metabolite concentration, nor nitrogen deficiency were necessary or sufficient to increase the proportion of unipolar budding cells. It is therefore unlikely that quorum sensing is the mechanism controlling the switch to filamentous growth in S. cerevisiae. Only a high concentration of the putative signalling molecule, 2-phenylethanol resulted in an increase in unipolar budding, but this concentration was not physiologically relevant. We suggest that the compound 2-phenylethanol acts through a toxicity mechanism, rather than quorum sensing, to induce filamentous growth.

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The intra-genus and inter-species quorum-sensing autoinducers exert distinct control over Vibrio cholerae biofilm formation and dispersal

10.1101/713685 ◽

2019 ◽

Author(s):

Andrew A. Bridges ◽

Bonnie L. Bassler

Keyword(s):

Quorum Sensing ◽

Vibrio Cholerae ◽

Cell Density ◽

Biofilm Formation ◽

Specific Information ◽

High Cell ◽

Coincidence Detector ◽

Sensing System ◽

Quorum Sensing System ◽

Cell Densities

AbstractVibrio cholerae possesses multiple quorum-sensing systems that control virulence and biofilm formation among other traits. At low cell densities, when quorum-sensing autoinducers are absent, V. cholerae forms biofilms. At high cell densities, when autoinducers have accumulated, biofilm formation is repressed and dispersal occurs. Here, we focus on the roles of two well-characterized quorum-sensing autoinducers that function in parallel. One autoinducer, called CAI-1, is used to measure vibrio abundance, and the other autoinducer, called AI-2, is a broadly-made universal autoinducer that is presumed to enable V. cholerae to assess the total bacterial cell density of the vicinal community. The two V. cholerae autoinducers funnel information into a shared signal relay pathway. This feature of the quorum-sensing system architecture has made it difficult to understand how specific information can be extracted from each autoinducer, how the autoinducers might drive distinct output behaviors, and in turn, how the bacteria use quorum sensing to distinguish self from other in bacterial communities. We develop a live-cell biofilm formation and dispersal assay that allows examination of the individual and combined roles of the two autoinducers in controlling V. cholerae behavior. We show that the quorum-sensing system works as a coincidence detector in which both autoinducers must be present simultaneously for repression of biofilm formation to occur. Within that context, the CAI-1 quorum-sensing pathway is activated when only a few V. cholerae cells are present, whereas the AI-2 pathway is activated only at much higher cell density. The consequence of this asymmetry is that exogenous sources of AI-2, but not CAI-1, contribute to satisfying the coincidence detector to repress biofilm formation and promote dispersal. We propose that V. cholerae uses CAI-1 to verify that some of its kin are present before committing to the high-cell-density quorum-sensing mode, but it is, in fact, the universal autoinducer AI-2, that sets the pace of the V. cholerae quorum-sensing program. This first report of unique roles for the different V. cholerae autoinducers suggests that detection of self fosters a distinct outcome from detection of other.

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Variation in Filamentous Growth and Response to Quorum-Sensing Compounds in Environmental Isolates of Saccharomyces cerevisiae

G3 Genes|Genome|Genetics ◽

10.1534/g3.119.400080 ◽

2019 ◽

Vol 9 (5) ◽

pp. 1533-1544 ◽

Cited By ~ 6

Author(s):

B. Adam Lenhart ◽

Brianna Meeks ◽

Helen A. Murphy

Keyword(s):

Saccharomyces Cerevisiae ◽

Quorum Sensing ◽

Filamentous Growth ◽

Environmental Isolates

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Can community-based signalling behaviour in Saccharomyces cerevisiae be called quorum sensing? A critical review of the literature

FEMS Yeast Research ◽

10.1093/femsyr/foz046 ◽

2019 ◽

Vol 19 (5) ◽

Cited By ~ 5

Author(s):

Michela Winters ◽

Nils Arneborg ◽

Rudi Appels ◽

Kate Howell

Keyword(s):

Saccharomyces Cerevisiae ◽

Quorum Sensing ◽

Cell Density ◽

Critical Concentration ◽

Threshold Value ◽

Fungal Species ◽

Signal Molecules ◽

Critical Signal ◽

Density Dependent ◽

Intercellular Signalling

ABSTRACTQuorum sensing is a well-described mechanism of intercellular signalling among bacteria, which involves cell-density-dependent chemical signal molecules. The concentration of these quorum-sensing molecules increases in proportion to cell density until a threshold value is exceeded, which triggers a community-wide response. In this review, we propose that intercellular signalling mechanisms can be associated with a corresponding ecological interaction type based on similarities between how the interaction affects the signal receiver and producer. Thus, we do not confine quorum sensing, a specific form of intercellular signalling, to only cooperative behaviours. Instead, we define it as cell-density-dependent responses that occur at a critical concentration of signal molecules and through a specific signalling pathway. For fungal species, the medically important yeast Candida albicans has a well-described quorum sensing system, while this system is not well described in Saccharomyces cerevisiae, which is involved in food and beverage fermentations. The more precise definition for quorum sensing proposed in this review is based on the studies suggesting that S. cerevisiae may undergo intercellular signalling through quorum sensing. Through this lens, we conclude that there is a lack of evidence to support a specific signalling mechanism and a critical signal concentration of these behaviours in S. cerevisiae, and, thus, these features require further investigation.

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Acetic Acid Acting as a Signal Molecule in Quorum Sensing System Enhances Production of 2,3-Butanediol in Saccharomyces Cerevisiae

10.21203/rs.3.rs-238949/v1 ◽

2021 ◽

Author(s):

Chi Zhang ◽

Tianqi Tong ◽

Jingping Ge

Keyword(s):

Saccharomyces Cerevisiae ◽

Acetic Acid ◽

Quorum Sensing ◽

Cell Density ◽

Acetolactate Synthase ◽

Production Method ◽

Threshold Concentration ◽

Original Strain ◽

Signal Molecule ◽

Acetic Acid Production

Abstract Objectives2,3-butanediol (2,3-BD) has been extensively used in chemical synthese. The traditional 2,3-BD production method has low yield and high cost. This study aimed to explore the use of acetic acid as a signal molecule to initiate a quorum sensing (QS) system in order to promote the production of 2,3-BD in Saccharomyces cerevisiae W141. ResultsWe found that the yield of 2,3-BD from S. cerevisiae W141 is proportional to the cell density. S. cerevisiae W141 does not produce 2,3-BD when cell density was lower than the threshold concentration (OD600 nm = 10 or cell density 4.4 × 108 CFU/mL). When 1.5 g/L acetic acid was added in the fermentation process, the yield of 2,3-BD was the highest reaching 3.01 ± 0.04 g/L (84 h). Subsequently, we found that S. cerevisiae W141 was co-cultured with Acetobacter pasteurianus Huniang 1.01 under the optimal conditions and the acetic acid production was increased by 76.7% and 30.6% compared with the original strain and the strain with 1.5 g/L acetic acid, respectively. In addition, the yield of 2,3-BD was respectively increased by 81.9% and 3.3%. The above results are attributable to the increased activity of acetolactate synthase (ILV2) and 2,3-BD dehydrogenase (BDH1) and the increase of the relative expression of ilv2 and bdh1 genes. ConclusionOur data showed that biosynthesis of 2,3-BD was regulated by acetic acid as a signaling molecule. Moreover the study provides a deeper understanding of the mechanisms underlying between acetic acid and 2,3-BD production.

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Elevated Growth of Saccharomyces cerevisiae ATH1 Null Mutants on Glucose Is an Artifact of Nonmatching Auxotrophies of Mutant and Reference Strains

Applied and Environmental Microbiology ◽

10.1128/aem.65.5.2267-2268.1999 ◽

1999 ◽

Vol 65 (5) ◽

pp. 2267-2268 ◽

Cited By ~ 10

Author(s):

Rohini Chopra ◽

Vishva Mitra Sharma ◽

K. Ganesan

Keyword(s):

Saccharomyces Cerevisiae ◽

Cell Density ◽

Control Strain ◽

Yeast Strains ◽

Acid Trehalase ◽

Cell Densities ◽

Reference Strains ◽

Null Mutants

ABSTRACT Yeast strains disrupted for ATH1, which encodes vacuolar acid trehalase, have been reported to grow to higher cell densities than reference strains. We showed that the increase in cell density is due to the URA3 gene introduced as a part of the disruption and concluded that the misinterpretation is a result of not using a control strain with matching auxotrophic markers.

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Variation in filamentous growth and response to quorum-sensing compounds in environmental isolates of Saccharomyces cerevisiae

10.1101/548099 ◽

2019 ◽

Author(s):

B. Adam Lenhart ◽

Brianna Meeks ◽

Helen A. Murphy

Keyword(s):

Saccharomyces Cerevisiae ◽

Quorum Sensing ◽

Natural Populations ◽

Filamentous Growth ◽

West African ◽

Natural Genetic Variation ◽

Pseudohyphal Growth ◽

Natural Isolates ◽

Candidate Loci ◽

Computational Image Analysis

AbstractIn fungi, filamentous growth is a major developmental transition that occurs in response to environmental cues. In diploid Saccharomyces cerevisiae, it is known as pseudohyphal growth and presumed to be a foraging mechanism. Rather than normal unicellular growth, multicellular filaments composed of elongated, attached cells spread over and into surfaces. This morphogenetic switch can be induced through quorum sensing with the aromatic alcohols phenylethanol and tryptophol. Most research investigating pseudohyphal growth has been conducted in a single lab background, Σ1278b. To investigate the natural variation in this phenotype and its induction, we assayed the diverse 100-genomes collection of environmental S. cerevisiae isolates. Using computational image analysis, we quantified the production of pseudohyphae and observed a large amount of variation. Unlike ecological niche, population membership was associated with pseudohyphal growth, with the West African population having the most. Surprisingly, most strains showed little or no response to exogenous phenylethanol or tryptophol. We also investigated the amount of natural genetic variation in pseudohyphal growth using a mapping population derived from a single, highly-heterozygous clinical isolate that contained as much phenotypic variation as the environmental panel. A bulk-segregant analysis uncovered five major peaks with candidate loci that have been implicated in the Σ1278b background. Our results indicate that the filamentous growth response is a generalized, highly variable phenotype in natural populations, while response to quorum sensing molecules is surprisingly rare. These findings highlight the importance of coupling studies in tractable lab strains with natural isolates in order to understand the relevance and distribution of well-studied traits.

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Filamentous growth of the budding yeast Saccharomyces cerevisiae induced by overexpression of the WHI2 gene

Microbiology ◽

10.1099/00221287-143-6-1867 ◽

1997 ◽

Vol 143 (6) ◽

pp. 1867-1876 ◽

Cited By ~ 16

Author(s):

P. A. Radcliffe ◽

K. M. Binley ◽

J. Trevethick ◽

M. Hall ◽

P. E. Sudbery

Keyword(s):

Saccharomyces Cerevisiae ◽

Budding Yeast ◽

Filamentous Growth ◽

Yeast Saccharomyces Cerevisiae

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Peptide signaling without feedback in signal production operates as a true quorum sensing communication system in Bacillus subtilis

Communications Biology ◽

10.1038/s42003-020-01553-5 ◽

2021 ◽

Vol 4 (1) ◽

Author(s):

Iztok Dogsa ◽

Mihael Spacapan ◽

Anna Dragoš ◽

Tjaša Danevčič ◽

Žiga Pandur ◽

...

Keyword(s):

Gene Expression ◽

Bacillus Subtilis ◽

Quorum Sensing ◽

Cell Density ◽

Communication System ◽

Communication Systems ◽

Feedback Loop ◽

Signal Molecules ◽

Specific Cell ◽

Sharp Transition

AbstractBacterial quorum sensing (QS) is based on signal molecules (SM), which increase in concentration with cell density. At critical SM concentration, a variety of adaptive genes sharply change their expression from basic level to maximum level. In general, this sharp transition, a hallmark of true QS, requires an SM dependent positive feedback loop, where SM enhances its own production. Some communication systems, like the peptide SM-based ComQXPA communication system of Bacillus subtilis, do not have this feedback loop and we do not understand how and if the sharp transition in gene expression is achieved. Based on experiments and mathematical modeling, we observed that the SM peptide ComX encodes the information about cell density, specific cell growth rate, and even oxygen concentration, which ensure power-law increase in SM production. This enables together with the cooperative response to SM (ComX) a sharp transition in gene expression level and this without the SM dependent feedback loop. Due to its ultra-sensitive nature, the ComQXPA can operate at SM concentrations that are 100–1000 times lower than typically found in other QS systems, thereby substantially reducing the total metabolic cost of otherwise expensive ComX peptide.

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