Two different Oenococcus oeni lineages are associated to either red or white wines in Burgundy: genomics and metabolomics insights

摘要

Oenococcus oeni is the bacterium most often associated with spontaneous malolactic fermentation (MLF) of wine. During MLF, malic acid is transformed into lactic acid and several metabolites are modified, modulating wine’s total acidity and improving its sensory properties. Previous works have suggested that certain genetic groups of O. oeni strains are associated to different kinds of products. In the present study we have spotted two groups of strains isolated mainly from Burgundy wines, one associated to red wines and the other to white wines. Sequencing 14 genomes of red and white wine strains revealed that they share a common ancestor that probably colonised two different substrates –red and white wine-associated environments–, diverging over time and disseminating to various regions. Their capacity to perform MLF and modify the volatile profile of wine was determined by fermenting a chardonnay wine and analysing its volatile fraction with a non-targeted metabolomics approach by GC-MS. The strains had a different impact on the volatile composition depending on their group of origin. These results show for the first time a correspondence between the product of origin of the strains and the volatile profile of the wines they produce. Furthermore, the genetic features that might be implied in these different phenotypes are examined. Introduction Microorganisms have, for millennia, played a central role in the discovery and development of fermented food by humans. It has been observed that the biogeography of microorganisms is influenced by human practices, as microorganisms have been domesticated to different food matrices that are produced in different regions (Legras et al., 2007; Douglas and Klaenhammer, 2010). Even for foods and beverages that are made nearly worldwide such as bread and wine, in which species are not always specific to a region or product, local variations in the biogeography of microorganisms have been observed in the form of genomic traces (Legras et al., 2007; Almeida et al., 2015). Even if Saccharomyces cerevisiae is the main yeast species responsible for the fermentation of wine, the contribution of the microbiological signature of non-Saccharomyces genera to the development of typical wine aroma has already been studied (Capozzi et al., 2015). The complexity of the ecosystem associated to oenological environments leads to a discussion about the possible existence of the so-called microbial terroir (Gilbert et al., 2014). Evidence suggests, at least for wine, that soil microbiome influences the grapevine-associated microbiota and that this microbial signature might be partially responsible for differential wine phenotypes (Bokulich et al., 2014; Zarraonaindia et al., 2015; Knight et al., 2015).Oenococcus oeni is the main species responsible for the malolactic fermentation (MLF) of wine, which normally follows the alcoholic fermentation (AF) produced by yeasts (Davis et al., 1986). Multilocus sequence typing analyses have revealed that the population of O. oeni is composed of a great diversity of strains that cluster in at least three main genetic groups, named A, B and C and a number of subgroups that sometimes correlate with their region (Chile, South Africa, Eastern France) or product of origin (cider, red and white wines, champagne) (Bilhère et al., 2009; Bridier et al., 2010). Genomic studies based on sequences of a few tens of strains have confirmed these genetic groups and they have suggested that ancestral O. oeni strains associated with fruits have been progressively domesticated to develop in cider and in wine, the strains of group A being presumably the best-adapted to wine (Borneman et al., 2012; Campbell-Sills et al., 2015). Recently, analysis of nearly 200 genomes, mostly from Australian isolates, showed that more than 60% of Australian isolates cluster in a closely-related group (a subgroup of A), suggesting that strains of this group may out-compete the other strains during fermentation or that they are well suited to Australian winemaking conditions (Sternes and Borneman, 2016). During MLF O. oeni converts malic acid into lactic acid and CO2, which makes wine softer in taste (Lonvaud-Funel, 1999). It also produces or degrades numerous secondary metabolites that can modify the fruity, vegetal or smoked aromas and contribute to the overall complexity of wine aroma (de Revel, 1999; Bartowsky, 2005; Vallet et al., 2008; Antalick et al., 2010; Antalick et al., 2012). Several studies have been made regarding the impact of different strains of O. oeni and other LAB in the composition of wine after MLF, both in primary and secondary metabolites (Pozo-Gayón et al., 2005; Ugliano and Moio, 2005; Lee et al., 2009a; Lee et al., 2009b; Hernandez-Orte et al., 2009; Costello et al., 2013; Sumby et al., 2013; Malherbe et al., 2013). However, it is still unknown whether strains of the same group have similar impacts on the quality of wines. In a recent survey of lactic acid bacter