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. 2025 Oct 15;73(41):26220-26231.
doi: 10.1021/acs.jafc.5c04823. Epub 2025 Oct 7.

First Evidence of Metabolically Active Intracellular Bacteria in Saccharomyces cerevisiae

Annabella Tramice  1 , Gianni Liti  2 , Annalaura Iodice  1 , Gennaro Roberto Abbamondi  1 , Federica Carlea  2 , Ernesto Petruzziello  3 , Adele Cutignano  1 , Debora Paris  1 , Carmine Iodice  1 , Matteo De Chiara  2 , Maria Aponte  3 , Francesca De Filippis  3   4 , Chiara Vischioni  2 , Andrea Motta  1 , Giuseppe Blaiotta  3   4 , Giuseppina Tommonaro  1
Affiliations

First Evidence of Metabolically Active Intracellular Bacteria in Saccharomyces cerevisiae

Annabella Tramice et al. J Agric Food Chem. .

Abstract

Quorum sensing (QS) is a cell-to-cell signaling system that takes place at a key concentration (quorum) of signal molecules and via a peculiar signaling pathway. Both bacteria and yeasts possess QS mechanisms, mediated by specific molecules (farnesol, tyrosol, 2-phenylethanol, tryptophol) in yeasts, and N-acylhomoserine lactones (AHLs) and modified oligopeptides in bacteria. Here, we report the first chemical evidence of bacterial QS activity in yeast Saccharomyces cerevisiae (OS3 and V5 strains) by UPLC-MS/MS identification of N-octanoyl- and N-decanoyl-L-homoserine lactones in cell-free culture media extracts. The AHLs' presence was unexpected, as they are produced exclusively by bacteria. Tyrosol, a yeast signal molecule, was identified and quantified by NMR analysis. Metataxonomic analysis suggested the existence inside S. cerevisiae cells of bacteria, including Firmicutes, Bacteroidota, and Proteobacteria. Our study paves the way for investigations into bacterial detection within S. cerevisiae cells and their role in biotechnological performance in the food fermentation fields.

Keywords: N-acylhomoserine lactones; Saccharomyces cerevisiae; metataxonomic analysis; quorum sensing; tyrosol.

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Figures

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(A) Monitoring of pH, viable yeast (log CFU/mL), and optical density (OD600) during the fermentation of Yeast Nitrogen Base without amino acids (YNBwAA) minimal medium containing 20 g/L dextrose by S. cerevisiae OS3. (B) Glucose (g/L) consumption and ethanol (g/L), glycerol (g/L), and succinic acid (g/L) production during the fermentation of Yeast Nitrogen Base without amino acids (YNBwAA) minimal medium containing 20 g/L of dextrose by S. cerevisiae OS3.
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Tyrosol production in the extracellular medium of S. cerevisiae OS3 during the fermentation process at different times (starting from 6 to 72 h). Within-sample statistical variation at different time points was evaluated with one-way repeated measures ANOVA with Bonferroni correction. Full results from multiple comparisons are reported in Table S2.
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TLC overlay of cell-free medium extracts of (A) S. cerevisiae OS3 strain at 12, 24, 48, and 72 h of growth and (B) S. cerevisiae V5 strain at 6 and 24 h of growth compared with the OS3 strain. A. tumefaciens NTL4 (pZLR4) was used as the bioreporter. AHLs signal molecules were detected by the presence of blue spots. Standards were N-(3-Oxohexanoyl)-l-homoserine lactone (3-oxo-C6-HSL) and N-(3-Oxodecanoyl)-l-homoserine lactone (3-oxo-C10-HSL).
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N-octanoyl l-homoserine lactone (C8-HSL) and N-decanoyl l-homoserine lactone (C10-HSL) production in the extracellular medium of S. cerevisiae during the fermentation process. Within-sample statistical variation at different time points was evaluated with one-way repeated measures ANOVA. For both N-octanoyl l-homoserine lactone (C8-HSL) and N-decanoyl L-homoserine lactone (C10-HSL), only the 12-h versus 48-h comparison showed a statistically significant difference, as reported in the corresponding bar plot (*p-adj < 0.05).
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Microscope analysis (1000× magnification) of moving bacteria-like bodies (MBLBs) inside the yeast cell of strain OS3 grown on YSM medium. (A,B) The red arrow in picture A points to the bacteria-like body moving inside the yeast cell. The pictures were taken a few seconds apart to show the active movement of the bacteria-like body. (C) As stress conditions increase (YPA medium 48 h), the presence in OS3 cells of MBLBs becomes greater. The figure shows them that they exit from the yeast cell, becoming empty. (D) The figure shows a cell of OS3 yeast surrounded by bacteria-like bodies (MBLBs) in potassium acetate, 96 h, 30 °C. Under severe stress conditions, caused by the absence of nutrients, the occurrence of dark dots (indicated by the arrow) within the cell can be seen. Dark dots surrounding the vacuole do not move and might consist of stress granules.
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A: Reaction with amylopectin; G: reaction with glycogen; L: reaction with laminarin; P: reaction with pullulan. V5: enzymatic digestion by crude protein enzymatic extracts from S. cerevisiae V5 at 24 h of growth in YNBwwAA medium. OS31: enzymatic digestion by crude protein enzymatic extracts from S. cerevisiae OS3 at 24 h of growth in YNBwwAA medium. OS32: enzymatic digestion by crude protein enzymatic extracts from S. cerevisiae OS3 at 118 h of growth in YSM medium.
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