Evolutionary Genomics of Lactic Acid Bacteria

Lactic Acid Bacteria (LAB) are responsible for many types of fermented foods and are part of our natural microbiota. The goal of this PhD was to leverage publicly available genomes of LAB to gain new insights into the evolutionary history and habitat-adaptation of these bacteria. To make this possible, important taxonomic and computational challenges were overcome.

Three groups of LAB were studied in the thesis. The first was the Lacticaseibacillus casei group: a cluster of closely related species with many applications as oral probiotics and in dairy fermentations, but with much confusion surrounding the classification of strains of the species L. casei, L. paracasei and L. zeae. Based on a comparison of all publicly available genomes from this group, the taxonomic confusion was cleared up, and a number of potentially habitat-relevant properties were identified that could discriminate between the species. For example, genes encoding catalases and putative epithelial adhesins were detected in L. casei genomes, and superoxide dismutase genes were found in L. paracasei genomes. The former were particularly relevant, because an L. casei strain with probiotic potential had previously been isolated from the upper respiratory tract of a healthy individual. Next, the family Lactobacillaceae was studied. For this purpose, a novel computational tool was developed to identify the core genes of a set of genomes in linear time. This tool was used to correct many species-level misclassifications of strains belonging to the family and to suggest mergers and splits of published species. For instance, a merger of the species Weissella thailandensis and Weissella jogaejeotgali was proposed, as well as a split of Ligilactobacillus aviarius. In addition, the genus Lactobacillus was split into 25 smaller genera and the families Leuconostocaceae and Lactobacillaceae were merged based on an analysis that included the use of signature genes to find biologically relevant clades. Finally, a novel tool was developed that could infer a pangenome (the collection of all gene families in a set of genomes) in near-linear time. This tool was then applied to create a pangenome database for the order Lactobacillales, which was subsequently explored to identify some trends in the evolution of these bacteria. For example, it was found that the number of core genes of species changes relatively slowly, and that genes encoding amino acid transporters experienced many duplications in the evolutionary history of the order.