Comparative Genomics of Streptococcus thermophilus Support Important Traits Concerning the Evolution, Biology and Technological Properties of the Species

Abstract

Streptococcus thermophilus is a major starter for the dairy industry with great economic importance. In this study we analyzed 23 fully sequenced genomes of S. thermophilus to highlight novel aspects of the evolution, biology and technological properties of this species. Pan/core genome analysis revealed that the species has an important number of conserved genes and that the pan genome is probably going to be closed soon. According to whole genome phylogeny and average nucleotide identity (ANI) analysis, most S. thermophilus strains were grouped in two major clusters (i.e., clusters A and B). More specifically, cluster A includes strains with chromosomes above 1.83 Mbp, while cluster B includes chromosomes below this threshold. This observation suggests that strains belonging to the two clusters may be differentiated by gene gain or gene loss events. Furthermore, certain strains of cluster A could be further subdivided in subgroups, i.e., subgroup I (ASCC 1275, DGCC 7710, KLDS SM, MN-BM-A02, and ND07), II (MN-BM-A01 and MN-ZLW-002), III (LMD-9 and SMQ-301), and IV (APC151 and ND03). In cluster B certain strains formed one distinct subgroup, i.e., subgroup I (CNRZ1066, CS8, EPS, and S9). Clusters and subgroups observed for S. thermophilus indicate the existence of lineages within the species, an observation which was further supported to a variable degree by the distribution and/or the architecture of several genomic traits. These would include exopolysaccharide (EPS) gene clusters, Clustered Regularly Interspaced Short Palindromic Repeats (CRISPRs)-CRISPR associated (Cas) systems, as well as restriction-modification (R-M) systems and genomic islands (GIs). Of note, the histidine biosynthetic cluster was found present in all cluster A strains (plus strain NCTC12958 T) but was absent from all strains in cluster B. Other loci related to lactose/galactose catabolism and urea metabolism, aminopeptidases, the majority of amino acid and peptide transporters, as well as amino acid biosynthetic pathways

Exopolysaccharides From Streptococcus thermophilus ST538 Modulate the Antiviral Innate Immune Response in Porcine Intestinal Epitheliocytes

“…Although the genome analysis of several S. thermophilus strains revealed variable sizes in the EPS gene clusters, the 5 and the 3 ends were highly conserved and their differences are located mainly in the middle of the clusters. Moreover, the epsA, epsB, epsC, and epsD genes were found at the 5 end in all the EPS gene clusters studied (Alexandraki et al, 2019).…”

“…In the EPS cluster, the genes in the 5 end are involved in the modulation and assembly machinery of polysaccharide biosynthesis. Those genes consist of five genes: epsA, epsB, epsC, epsD, and epsE, which display the highest level of overall conservation among different Streptococcus strains (Zeidan et al, 2017;Jolly and Stingele, 2012;Goh et al, 2011;Alexandraki et al, 2019). The epsC gene encodes a membranebound protein with a cytoplasmic C-terminal domain required for kinase activation.…”

“…Structurally, the EPS produced by S. thermophilus are heteropolysaccharides made up of oligosaccharide repeating unit synthetized in the cytoplasm by the action of a number of glycosyltransferases and branched chains containing glucose and galactose, rhamnose and sometimes N-acetyl-glucosamine and fucose (Doco et al, 1990;Petit et al, 1991;Dan et al, 2009). Genome-scale studies revealed that the EPS biosynthetic pathway in S. thermophilus involves the sugar uptake system, nucleotide sugar synthesis, polysaccharide synthesis, and export of EPS, which are controlled by several housekeeping genes and a cluster of EPS-related genes (Laws et al, 2001;Wu et al, 2014;Cui et al, 2017;Alexandraki et al, 2019;Xiong et al, 2019). In lactic acid bacteria (LAB), the typical EPS gene cluster was described to contain five highly conserved genes epsA, epsB, epsC, epsD, and epsE, and a variable region, which includes the genes for polymerases, flippases, and a variable number of glycosyltransferases and other modifying enzymes [reviewed in Zeidan et al (2017)].…”

“…It has been shown that the phosphoregulatory system, constituted by epsB, epsC, and epsD, is responsible for the control of the polysaccharide assembly machinery (Yother, 2011;Grangeasse, 2016). Recent genomic studies have demonstrated a similar organization in the EPS clusters of S. thermophilus (Alexandraki et al, 2019). Although the genome analysis of several S. thermophilus strains revealed variable sizes in the EPS gene clusters, the 5 and the 3 ends were highly conserved and their differences are located mainly in the middle of the clusters.…”

Cell‐envelope proteinases from lactic acid bacteria: Biochemical features and biotechnological applications

“…The genomes of Lb. delbrueckii species have been well studies (Alexandraki et al., 2019; Alexandraki et al., 2017; Hao et al., 2011; Kanmani et al., 2018; Makarova et al., 2006; Van de Guchte et al., 2006), and the presence and sequence of CEP genes such as prtB (Gilbert et al., 1996) and prtL (Hebert et al., 2013) have been identified in Lb. delbrueckii subsp.…”