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Summary  We proposed a novel phenomic approach to track the effect of short‐term exposures of  Lactiplantibacillus plantarum  and  Leuconostoc pseudomesenteroides  to environmental pressure induced by brewers' spent grain (BSG)‐derived saccharides. Water‐soluble BSG‐based medium (WS‐BSG) was chosen as model system. The environmental pressure exerted by WS‐BSG shifted the phenotypes of bacteria in species‐ and strains‐dependent way. The metabolic drift was growth phase‐dependent and likely underlay the diauxic profile of organic acids production by bacteria in response to the low availability of energy sources. Among pentosans, metabolism of arabinose was preferred by  L .  plantarum  and xylose by  Leuc .  pseudomesenteroides  as confirmed by the overexpression of related genes. Bayesian variance analysis showed that phenotype switching towards galactose metabolism suffered the greatest fluctuation in  L .  plantarum . All lactic acid bacteria strains utilized more intensively sucrose and its plant‐derived isomers. Sucrose‐6‐phosphate activity in  Leuc .  pseudomesenteroides  likely mediated the increased consumption of raffinose. The increased levels of some phenolic compounds suggested the involvement of 6‐phospho‐β‐glucosidases in β‐glucosides degradation. Expression of genes encoding β‐glucoside/cellobiose‐specific EII complexes and phenotyping highlighted an increased metabolism for cellobiose. Our reconstructed metabolic network will improve the understanding of how lactic acid bacteria may transform BSG into suitable food ingredients.

How water‐soluble saccharides drive the metabolism of lactic acid bacteria during fermentation of brewers' spent grain