Metabolic plasticity of Oenococcus oeni driven by strain diversity and wine matrix composition

Abstract

Oenococcus oeni is an essential microorganism in winemaking due to its role in malolactic fermentation (MLF). Genetic variability among strains within this species leads to marked differences in metabolic capacities and adaptive potential, which strongly influence MLF performance. The metabolic behavior of O. oeni is therefore of particular interest, as these diverse strains must operate within the complex wine matrix. Investigating how different strains express these metabolic traits provides valuable insight into the mechanisms that shape wine evolution during MLF. To investigate how this diversity translates into distinct metabolic outputs, eight strains were inoculated into four red wine matrices differing in variety (Pinot Noir, Merlot) and in their adjusted or unadjusted pH and L-malic acid levels. L-malic acid degradation kinetics were monitored and integrated with high resolution mass spectrometry (HRMS) exometabolomic profiling. This combined approach allows a comprehensive characterization of strain-dependent metabolic signatures. Multivariate analyses revealed that, beyond a shared metabolic foundation associated with stress adaptation, strains deployed divergent metabolic programs. Differences have been observed in central carbon fluxes, membrane-associated responses and the transformation of phenolic compounds. These contrasted behaviors highlight the capacity of O. oeni to modulate its metabolic activity depending on both intrinsic genetic traits and extrinsic environmental factors. These differences reflect the modulation of metabolic activity driven by both genetic background and wine matrix composition, with polyphenols and their derivatives emerging as major discriminant features and potential markers of malolactic fermentation outcomes. Overall, the results demonstrate that the interplay between microbial genotype and wine composition governs the metabolic trajectories of O. oeni during malolactic fermentation, highlighting the strain-dependent plasticity that can influence red wine chemical profiles. These findings reinforce the value of untargeted metabolomics for capturing the complexity of microbial activity in wine and open perspectives for selecting strains according to desired enological outcomes.