Characterization of the First Virulent Phage Infecting Oenococcus oeni, the Queen of the Cellars

Abstract

There has been little exploration of how phages contribute to the diversity of the bacterial community associated with winemaking and may impact fermentations and product quality. Prophages of Oenococcus oeni, the most common species of lactic acid bacteria (LAB) associated with malolactic fermentation of wine, have been described, but no data is available regarding phages of O. oeni with true virulent lifestyles. The current study reports on the incidence and characterization of the first group of virulent oenophages named Vinitor, isolated from the enological environment. Vinitor phages are morphologically very similar to siphoviruses infecting other LAB. Although widespread during winemaking, they are more abundant in musts than temperate oenophages. We obtained the complete genomic sequences of phages Vinitor162 and Vinitor27, isolated from white and red wines, respectively. The assembled genomes shared 97.6% nucleotide identity and belong to the same species. Coupled with phylogenetic analysis, our study revealed that the genomes of Vinitor phages are architecturally mosaics and represent unique combinations of modules amongst LAB infecting-phages. Our data also provide some clues to possible evolutionary connections between Vinitor and (pro)phages associated to epiphytic and insect-related bacteria.

Structure and Topology Prediction of Phage Adhesion Devices Using AlphaFold2: The Case of Two Oenococcus oeni Phages

“…In previous studies, we have shown that the OE33PA adhesion device has three components: Dit, Tal, and RBP. Meanwhile, only two components, Dit and Tal, make up that of Vinitor162 [ 4 ] ( Figure 1 ).…”

“…Vinitor162 has only two putative proteins building its adhesion device: a Dit and a long and extended Tal [ 4 ].…”

“…The assembly of the Tal C-terminal end was produced with SymmDock for the β -prisms and β -helices domains, as well as with AlphaFold2 for the chaperone domain. These modules were placed according to their sequence order along the Tal extension, as viewed by negative staining electron microscopy (nsEM) [ 4 ]. The figures of the OE33PA and Vinitor162 adhesion device topology predictions were prepared with ChimeraX [ 26 ].…”

“…This is true for fermented beverages, as exemplified by the emblematic and economically important field of winemaking, which relies heavily on the LAB species Oenococcus oeni. Recently, we have shown that representative phages that infect O. oeni possess host-binding devices with distinct compositions and morphologies [ 4 , 5 ] that differ from those of lactococcal and streptococcal phages. Moreover, wine polyphenolic compounds (PCs), which are abundant in the O. oeni ecological niche, can interfere with the phage infection process, as they may mimic some components of host cell wall polysaccharides (CWPS) [ 5 ].…”

“…Tals can be short, with a minimal length of 330 to 380 residues [ 11 ], or very long, with as many as 2000 residues [ 2 ]. They often harbor several CBMs along their extension and at their extremity [ 4 , 12 , 13 ]. This assembly can be completed by other proteins co-involved in CWPS binding, including one or several receptor-binding proteins (RBP) [ 2 , 7 , 14 ].…”