Mutations and genomic islands can explain the strain dependency of sugar utilization in 21 strains of Propionibacterium freudenreichii

Propionibacterium freudenreichii (PF) is an actinobacterium used in cheese technology and for its probiotic properties. PF can grow on a variety of carbon and nitrogen sources. The aim of this work was to discover the genetic basis for strain-dependent traits related to its ability to use specific carbon sources. Twenty-one strains were sequenced. Each gene was attributed to either the core genome or an accessory genome. The ability of the 21 strains to degrade 50 different sugars was evaluated. Thirty-three sugars were degraded by none of the sequenced strains whereas eight sugars were degraded by all of them. The corresponding genes were present in the core genome. Lactose, melibiose were only used by some strains. The presence/absence of genes responsible for carbon uptake and degradation correlated well with the phenotypes and was in line the metabolic pathways described previously in other species. We also considered the genetic origin (transduction, rearrangement) of the corresponding genomic islands. Ribose and gluconate were to a greater or lesser extent (quantitative phenotype) degraded by some strains. For these sugars, the phenotypes correlated with the premature appearance of a stop codon interrupting protein synthesis, preventing the catabolism of corresponding sugar. These results illustrate (i) the power of correlation studies to discover the genetic basis of binary strain-dependent traits, and (ii) the plasticity of PF chromosomes, probably resulting from horizontal transfers, duplications, transpositions and an accumulation of mutations.