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

Abstract

BackgroundPropionibacterium freudenreichii (PF) is an actinobacterium used in cheese technology and for its probiotic properties. PF is also extremely adaptable to several ecological niches and 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. High-throughput sequencing technologies were ideal for this purpose as they have the potential to decipher genomic diversity at a moderate cost.Results21 strains of PF were sequenced and the genomes were assembled de novo. Scaffolds were ordered by comparison with the complete reference genome CIRM-BIA1, obtained previously using traditional Sanger sequencing. Automatic functional annotation and manual curation were performed. 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 and xylitol were only used by some strains. In this case, the presence/absence of genes responsible for carbon uptake and degradation correlated well with the phenotypes, with the exception of xylitol. Furthermore, the simultaneous presence of these genes 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 degraded to a greater or lesser extent (quantitative phenotype) by some strains. For these sugars, the phenotypes could not be explained by the presence/absence of a gene but correlated with the premature appearance of a stop codon interrupting protein synthesis and preventing the catabolism of corresponding carbon sources.ConclusionThese 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. Knowledge of the genetic basis of nitrogen and sugar degradation opens up new strategies for the screening of PF strain collections to enable optimum cheese starter, probiotic and white biotechnology applications.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1467-7) contains supplementary material, which is available to authorized users.

Carbohydrate metabolism in Oenococcus oeni: a genomic insight

“…Additional analyzes were required in many other cases, due to probable complementation phenomena (in the case of trehalose, arabinose, ribose) or to multiple metabolic pathways (in the case of glucose, fructose or cellobiose). Siezen et al [34], Bottaciani et al [35] and Loux et al [36] had already raised this problem with other LAB species. Moreover, sugar carriers are very numerous in O. oeni [19].…”

“…plantarum [34, 38, 39] or into large genomic islands as capsular exopolysaccharide gene clusters [25]. Moreover, as in other genera [35, 36], the genes are frequently organized in gene clusters encoding two or more functions associated with a specific carbohydrate metabolism, but several distant clusters on the chromosome are often required. This highly conserved scattered chromosomal distribution is generally found in species or subspecies in which all strains share very similar ecological niches and in which no individual evolved to colonize new environments [36, 40, 41].…”

“…This may protect the bacteria from losing several carbohydrate degradation abilities through a single recombination event. As proposed for other species [36, 37, 40], the genetic origin of the phenotypes observed in O. oeni may include majors events that led to the global evolution of the species (acquisition of the arabinose, trehalose and maltose clusters, and of the rescue glucose uptake systems), but also marginal events, such as acquisition/loss of genes in a limited number of strains (xylose cluster, pts fru , manC , levO) and many punctual mutations that lead to phenotype loss without gene loss. The list of gene clusters conserved or acquired at the emergence of O. oeni species suggests that the gradual specialization of Oenococci to the wine environment required mainly the maintenance of catabolic activities towards glucose, ribose, trehalose, mannose, cellobiose, melibiose, maltose and arabinose.…”

Hyperconcentrated Sweet Whey, a New Culture Medium That Enhances Propionibacterium freudenreichii Stress Tolerance

“…shermanii ITG P20, used in this study, is able to use various substrates as carbon and energy sources for growth. Carbohydrates, including sucrose, lactose, glucose, galactose, inositol, erythritol, adonitol, and esculine, may be used (35), as well as amino acids, glycerol, or its preferred carbon source, which is lactate (contained in the reference YEL growth medium). Within dairy products, it can thus utilize either lactose, the major milk carbohydrate, or lactate, resulting from lactic acid fermentation.…”

Strain-to-strain differences within lactic and propionic acid bacteria species strongly impact the properties of cheese–A review

“…The adaptation to diverse ecological niches is genetically determined by the acquisition of new genes by HGT, in parallel to the decay and loss of non-essential genes as highlighted by comparative genomic analysis in LAB and PAB (Cai et al 2009;Cavanagh et al 2015;Kelleher et al 2015;Loux et al 2015;Papadimitriou et al 2015). Many examples of HGT in food-related LAB species have been reported (Rossi et al 2014).…”