Limits...
Phylogenomic Analysis of Oenococcus oeni Reveals Specific Domestication of Strains to Cider and Wines.

Campbell-Sills H, El Khoury M, Favier M, Romano A, Biasioli F, Spano G, Sherman DJ, Bouchez O, Coton E, Coton M, Okada S, Tanaka N, Dols-Lafargue M, Lucas PM - Genome Biol Evol (2015)

Bottom Line: A study on the orthologs and single nucleotide polymorphism contents of the genetic groups revealed that the domestication of some strains to products such as cider, wine, or champagne, is reflected at the genetic level.While group A strains proved to be predominant in wine and to form subgroups adapted to specific types of wine such as champagne, group B strains were found in wine and cider.The results suggest that ancestral O. oeni strains were adapted to low-ethanol containing environments such as overripe fruits, and that they were domesticated to cider and wine, with group A strains being naturally selected in a process of further domestication to specific wines such as champagne.

View Article: PubMed Central - PubMed

Affiliation: Univ. Bordeaux, ISVV, EA 4577 Œnologie, Villenave d'Ornon, France Research and Innovation Centre, Fondazione Edmund Mach, San Michele all'Adige, Italy.

Show MeSH

Related in: MedlinePlus

Phylogenomic reconstruction of O. oeni and its closest relatives by ANIb. The 50 O. oeni strains were branched to four strains of O. kitaharae, from which three were sequenced for this study, and three strains of L. mesenteroides, of which one corresponds to the cremoris subspecies (Lmc) and the other two correspond to mesenteroides (Lmm). The branches that separate the species were truncated for better display, which is represented by pointed lines. Numbers over the pointed lines indicate the total length of the respective branches. Distance is shown in terms of percentage of divergence according to ANI.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4494047&req=5

evv084-F4: Phylogenomic reconstruction of O. oeni and its closest relatives by ANIb. The 50 O. oeni strains were branched to four strains of O. kitaharae, from which three were sequenced for this study, and three strains of L. mesenteroides, of which one corresponds to the cremoris subspecies (Lmc) and the other two correspond to mesenteroides (Lmm). The branches that separate the species were truncated for better display, which is represented by pointed lines. Numbers over the pointed lines indicate the total length of the respective branches. Distance is shown in terms of percentage of divergence according to ANI.

Mentions: In order to evaluate the evolutionary relationships between O. oeni strains and between O. oeni and other species, an ANI tree was constructed using BLAST algorithm, known as ANIb (fig. 4). The tree was outgrouped by including three genomes of Leuconostoc mesenteroides subspecies mesenteroides and cremoris, and four genomes of the sister species O. kitaharae (table 1). Due to differences of sensibility between MUMmer and BLAST algorithms, discrepancies between trees constructed by both methods become more evident as genomes start to diverge (ANI < 90%). ANIm results are more robust when analyzing closely related genomes, but ANIb is preferable in this case since the compared genomes can have an ANI as low as 65%. A comparison of the previously published genome of O. kitaharae (Borneman et al. 2012b) and the three newly made genomes reported in this study reveals that they are rather homogenous at the sequence level in comparison to those of O. oeni. This is not surprising since all four strains were isolated from the same sample (Endo and Okada 2006), even if it is not uncommon to find genetically different strains in the same environment. The branch lengths of the reconstructed tree show that O. oeni strains are more divergent than strains of L. mesenteroides at the sequence level, although the latter are considered to form two subspecies (Hemme and Foucaud-Scheunemann 2004). However, sequence similarity alone is not enough to determine whether a set of strains corresponds to different (sub)species or not. In one hand, in order to be considered as a single species the genomes must share at least greater than 95% ANI (Thompson et al. 2013), which corresponds to the case of O. oeni. In the other hand, phenotypic characteristics can be at least partially predicted from genomic data in order to further classify the strains of a species (Amaral et al. 2014). This might be the case of the strains isolated from champagne and of IOEB_C52. The former shares a set of 27 unique SNP that generate truncate or longer proteins, or that skip the start codon. The affected genes are implied in diverse metabolic pathways which could at least partially explain this strains’ adaptation to champagne. They also have a cellulose 1,4-beta-cellobiosidase enzyme that does not match with the other strains according to the orthoMCL analysis. The strain IOEB_C52, at the sequence level, appears at the most basal position among O. oeni strains and has a set of 65 unique genes, some of them possibly explaining some of its technologic properties. However, because this is the only individual representing its putative group, the evidence to confirm that it might belong to a different class is weak. From the evolutionary point of view, this strain might represent a genetic group that preceded the advent of groups A and B, because domestication is also driven by a loss of genetic functions and a specialization. Interestingly this strain was isolated from cider as three other strains from group B. It is not surprising that O. oeni develops well in cider because cider is rather similar as wine regarding stress parameters: acidity, ethanol, polyphenols, and available substrates (sugars, malate, and citrate). The main difference is probably the total level of alcohol that rarely exceeds 6% in cider, whereas it is usually 11–14% in wine (Picinelli et al. 2000). Bacteria that naturally occur on fruits are exposed to low ethanol levels when overmaturated fruits are decomposed by the action of molds and yeasts. Therefore it is possible that the most ancient O. oeni strains, represented by strain IOEB_C52, were adapted to low ethanol containing environments, and that some strains of group B and most strains of group A have evolved to tolerate higher ethanol concentrations and to survive in wine. This likely represents a case of strain domestication because the wine environment exists only due to human activity. Domestication of O. oeni has been already reported (Douglas and Klaenhammer 2010); however, our results suggest that this domestication has not reached to the same level the strains of groups A, B, and C, which is reflected at the genomic level and confirmed by the population structure analysis. Because they group together, O. oeni strains from champagne have probably evolved a supplementary adaptive ability that could be the tolerance to the extreme acidity of this type of wine (pH ∼3.0). Domestication of other microorganisms in wine has also been observed for some species belonging to the Saccharomyces sensu stricto complex (Sicard and Legras 2011), such as Saccharomyces cerevisiae (Fay and Benavides 2005; Legras et al. 2007; Albertin et al. 2009) and Saccharomyces uvarum (Almeida et al. 2014).Fig. 4.—


Phylogenomic Analysis of Oenococcus oeni Reveals Specific Domestication of Strains to Cider and Wines.

Campbell-Sills H, El Khoury M, Favier M, Romano A, Biasioli F, Spano G, Sherman DJ, Bouchez O, Coton E, Coton M, Okada S, Tanaka N, Dols-Lafargue M, Lucas PM - Genome Biol Evol (2015)

Phylogenomic reconstruction of O. oeni and its closest relatives by ANIb. The 50 O. oeni strains were branched to four strains of O. kitaharae, from which three were sequenced for this study, and three strains of L. mesenteroides, of which one corresponds to the cremoris subspecies (Lmc) and the other two correspond to mesenteroides (Lmm). The branches that separate the species were truncated for better display, which is represented by pointed lines. Numbers over the pointed lines indicate the total length of the respective branches. Distance is shown in terms of percentage of divergence according to ANI.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4494047&req=5

evv084-F4: Phylogenomic reconstruction of O. oeni and its closest relatives by ANIb. The 50 O. oeni strains were branched to four strains of O. kitaharae, from which three were sequenced for this study, and three strains of L. mesenteroides, of which one corresponds to the cremoris subspecies (Lmc) and the other two correspond to mesenteroides (Lmm). The branches that separate the species were truncated for better display, which is represented by pointed lines. Numbers over the pointed lines indicate the total length of the respective branches. Distance is shown in terms of percentage of divergence according to ANI.
Mentions: In order to evaluate the evolutionary relationships between O. oeni strains and between O. oeni and other species, an ANI tree was constructed using BLAST algorithm, known as ANIb (fig. 4). The tree was outgrouped by including three genomes of Leuconostoc mesenteroides subspecies mesenteroides and cremoris, and four genomes of the sister species O. kitaharae (table 1). Due to differences of sensibility between MUMmer and BLAST algorithms, discrepancies between trees constructed by both methods become more evident as genomes start to diverge (ANI < 90%). ANIm results are more robust when analyzing closely related genomes, but ANIb is preferable in this case since the compared genomes can have an ANI as low as 65%. A comparison of the previously published genome of O. kitaharae (Borneman et al. 2012b) and the three newly made genomes reported in this study reveals that they are rather homogenous at the sequence level in comparison to those of O. oeni. This is not surprising since all four strains were isolated from the same sample (Endo and Okada 2006), even if it is not uncommon to find genetically different strains in the same environment. The branch lengths of the reconstructed tree show that O. oeni strains are more divergent than strains of L. mesenteroides at the sequence level, although the latter are considered to form two subspecies (Hemme and Foucaud-Scheunemann 2004). However, sequence similarity alone is not enough to determine whether a set of strains corresponds to different (sub)species or not. In one hand, in order to be considered as a single species the genomes must share at least greater than 95% ANI (Thompson et al. 2013), which corresponds to the case of O. oeni. In the other hand, phenotypic characteristics can be at least partially predicted from genomic data in order to further classify the strains of a species (Amaral et al. 2014). This might be the case of the strains isolated from champagne and of IOEB_C52. The former shares a set of 27 unique SNP that generate truncate or longer proteins, or that skip the start codon. The affected genes are implied in diverse metabolic pathways which could at least partially explain this strains’ adaptation to champagne. They also have a cellulose 1,4-beta-cellobiosidase enzyme that does not match with the other strains according to the orthoMCL analysis. The strain IOEB_C52, at the sequence level, appears at the most basal position among O. oeni strains and has a set of 65 unique genes, some of them possibly explaining some of its technologic properties. However, because this is the only individual representing its putative group, the evidence to confirm that it might belong to a different class is weak. From the evolutionary point of view, this strain might represent a genetic group that preceded the advent of groups A and B, because domestication is also driven by a loss of genetic functions and a specialization. Interestingly this strain was isolated from cider as three other strains from group B. It is not surprising that O. oeni develops well in cider because cider is rather similar as wine regarding stress parameters: acidity, ethanol, polyphenols, and available substrates (sugars, malate, and citrate). The main difference is probably the total level of alcohol that rarely exceeds 6% in cider, whereas it is usually 11–14% in wine (Picinelli et al. 2000). Bacteria that naturally occur on fruits are exposed to low ethanol levels when overmaturated fruits are decomposed by the action of molds and yeasts. Therefore it is possible that the most ancient O. oeni strains, represented by strain IOEB_C52, were adapted to low ethanol containing environments, and that some strains of group B and most strains of group A have evolved to tolerate higher ethanol concentrations and to survive in wine. This likely represents a case of strain domestication because the wine environment exists only due to human activity. Domestication of O. oeni has been already reported (Douglas and Klaenhammer 2010); however, our results suggest that this domestication has not reached to the same level the strains of groups A, B, and C, which is reflected at the genomic level and confirmed by the population structure analysis. Because they group together, O. oeni strains from champagne have probably evolved a supplementary adaptive ability that could be the tolerance to the extreme acidity of this type of wine (pH ∼3.0). Domestication of other microorganisms in wine has also been observed for some species belonging to the Saccharomyces sensu stricto complex (Sicard and Legras 2011), such as Saccharomyces cerevisiae (Fay and Benavides 2005; Legras et al. 2007; Albertin et al. 2009) and Saccharomyces uvarum (Almeida et al. 2014).Fig. 4.—

Bottom Line: A study on the orthologs and single nucleotide polymorphism contents of the genetic groups revealed that the domestication of some strains to products such as cider, wine, or champagne, is reflected at the genetic level.While group A strains proved to be predominant in wine and to form subgroups adapted to specific types of wine such as champagne, group B strains were found in wine and cider.The results suggest that ancestral O. oeni strains were adapted to low-ethanol containing environments such as overripe fruits, and that they were domesticated to cider and wine, with group A strains being naturally selected in a process of further domestication to specific wines such as champagne.

View Article: PubMed Central - PubMed

Affiliation: Univ. Bordeaux, ISVV, EA 4577 Œnologie, Villenave d'Ornon, France Research and Innovation Centre, Fondazione Edmund Mach, San Michele all'Adige, Italy.

Show MeSH
Related in: MedlinePlus