Evolution of lactic acid bacteria as revealed by comparative genomics of carbohydrate metabolism

Lactic acid bacteria (LAB) are a functional group of bacteria crucial in human nutrition for their role in fermented food production and their presence in gastro-intestinal tract. Co-evolution and niche-adaptation of LAB have been extensively analysed in several phylogenomic studies, thanks to the availability of complete genome sequences. The aim of this study was to analyze the evolution of LAB from a different viewpoint: the comparative analysis of the metabolic pathways related to carbohydrate metabolism. The analysis was performed on 40 LAB genomes belonging to strains of Enterococcaceae, Lactobacillaceae, Leuconostocaceae and Streptococcaceae families. A reference phylogenetic tree was inferred from the concatenation of 42 ribosomal proteins; moreover 45 genes belonging to Embden-Meyerhof-Parnas pathway (or glycolysis, EMPP) and pentose phosphate pathway (PPP) were analyzed in terms of presence/absence, number of paralogs and their use as phylogenetic markers. Phylogenetic analysis confirmed the paraphyly of Lactobacillaceae while the analysis of EMPP and PPP genes distribution revealed the occurrence of lineage-specific trends of gene loss/gain within the two metabolic pathways in LAB. In addition, the investigation of EMPP and PPP as structures resulting from different evolutionary processes provided new information concerning the genetic bases of heterofermentative/homofermentative metabolism. Overall, our analyses offered a better comprehension of the molecular mechanisms and the evolutionary processes that have led to contemporary biochemical pathways in LAB representatives. The same approach could then be applied to other metabolic pathways in order to set up directed evolution experiments to improve production of LAB peculiar components with health-promoting or probiotic effects