Distribution and Functions of Phosphotransferase System Genes in the Genome of the Lactic Acid Bacterium Oenococcus oeni

Abstract

Oenococcus oeni, the lactic acid bacterium primarily responsible for malolactic fermentation in wine, is able to grow on a large variety of carbohydrates, but the pathways by which substrates are transported and phosphorylated in this species have been poorly studied. We show that the genes encoding the general phosphotransferase proteins, enzyme I (EI) and histidine protein (HPr), as well as 21 permease genes (3 isolated ones and 18 clustered into 6 distinct loci), are highly conserved among the strains studied and may form part of the O. oeni core genome. Additional permease genes differentiate the strains and may have been acquired or lost by horizontal gene transfer events. The core pts genes are expressed, and permease gene expression is modulated by the nature of the bacterial growth substrate. Decryptified O. oeni cells are able to phosphorylate glucose, cellobiose, trehalose, and mannose at the expense of phosphoenolpyruvate. These substrates are present at low concentrations in wine at the end of alcoholic fermentation. The phosphotransferase system (PTS) may contribute to the perfect adaptation of O. oeni to its singular ecological niche.

Carbohydrate metabolism in Oenococcus oeni: a genomic insight

“…The genes mfs0819 and mfs1574 were shown to be highly overexpressed during cultures of O. oeni B1 (no genome available) on glucose, and the glucose uptake activity of the encoded proteins was demonstrated by heterologous expression in Bacillus subtilis [21]. The gene mfs0136 was slightly overexpressed in the presence of glucose, but the activity of the encoded protein has not been demonstrated [22]. The manB operon was shown to be overexpressed during cultures on glucose and fructose [21, 22].…”

“…The gene mfs0136 was slightly overexpressed in the presence of glucose, but the activity of the encoded protein has not been demonstrated [22]. The manB operon was shown to be overexpressed during cultures on glucose and fructose [21, 22]. In Champagne strains, which exhibit a particularly slow growth compared to the others (μ ≈ 0.35 day −1 against 0.6–0.7 day −1 for most strains), several genes associated with glucose catabolism seem singular: the gene mfs1574 is truncated while Mfs0136 and ManB display specific protein sequences.…”

“…The manA operon encoded a potentially active and not singular permease in 3 of these 5 negative strains (B16, IOEB_0205 and AWRI_B548), and it was truncated in a positive strain (ATCC_BAA-1163), which makes it unlikely that ManA is involved in mannose uptake. By opposition, there was a singular ManB permease (specific mutation in the IIC subunit) in the 5 mannose negative strains, which suggests that mannose transport could be driven by ManB , despite the fact that both manA and manB are overexpressed in the presence of mannose [22]. …”

“…Meanwhile, Kim et al [21] identified the genes encoding transport proteins whose expression was induced in the presence of glucose or fructose. Jamal et al [22] identified the pts genes induced in the presence of glucose and fructose but also cellobiose, trehalose and mannose. This last study also pointed out the high degree of pts gene conservation in the species, by comparing the 14 genome sequences available at the time.…”

Genomics of Lactic Acid Bacteria

“…Our preliminary analysis indicated that the number of PTS-related proteins, particularly the PTS enzyme II genes for fructose and mannose family, significantly varied in three completed L. casei genomes . In contrast, genes encoding PTS systems are highly conserved in O. oeni strains (Jamal et al 2013). L. casei is a versatile microorganism that can be found in various niches, whereas O. oeni is indigenous to wine or similar niches.…”