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Comparative analysis of the Oenococcus oeni pan genome reveals genetic diversity in industrially-relevant pathways.

Borneman AR, McCarthy JM, Chambers PJ, Bartowsky EJ - BMC Genomics (2012)

Bottom Line: These benefits are realised primarily through catalysing malolactic fermentation, but also through imparting other positive sensory properties.While any single strain of O. oeni was shown to contain around 1800 protein-coding genes, in-depth comparative annotation based on genomic synteny and protein orthology identified over 2800 orthologous open reading frames that comprise the pan genome of this species, and less than 1200 genes that make up the conserved genomic core present in all of the strains.This data is vital to understanding and harnessing the phenotypic variation present in this economically-important species.

View Article: PubMed Central - HTML - PubMed

Affiliation: The Australian Wine Research Institute, Glen Osmond, South Australia 5064, Australia. anthony.borneman@awri.com.au

ABSTRACT

Background: Oenococcus oeni, a member of the lactic acid bacteria, is one of a limited number of microorganisms that not only survive, but actively proliferate in wine. It is also unusual as, unlike the majority of bacteria present in wine, it is beneficial to wine quality rather than causing spoilage. These benefits are realised primarily through catalysing malolactic fermentation, but also through imparting other positive sensory properties. However, many of these industrially-important secondary attributes have been shown to be strain-dependent and their genetic basis it yet to be determined.

Results: In order to investigate the scale and scope of genetic variation in O. oeni, we have performed whole-genome sequencing on eleven strains of this bacterium, bringing the total number of strains for which genome sequences are available to fourteen. While any single strain of O. oeni was shown to contain around 1800 protein-coding genes, in-depth comparative annotation based on genomic synteny and protein orthology identified over 2800 orthologous open reading frames that comprise the pan genome of this species, and less than 1200 genes that make up the conserved genomic core present in all of the strains. The expansion of the pan genome relative to the coding potential of individual strains was shown to be due to the varied presence and location of multiple distinct bacteriophage sequences and also in various metabolic functions with potential impacts on the industrial performance of this species, including cell wall exopolysaccharide biosynthesis, sugar transport and utilisation and amino acid biosynthesis.

Conclusions: By providing a large cohort of sequenced strains, this study provides a broad insight into the genetic variation present within O. oeni. This data is vital to understanding and harnessing the phenotypic variation present in this economically-important species.

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Variations in sugar utilisation pathways in O. oeni. A. The predicted pathway for the assimilation of L-arabinose and L-xylulose in O. oeni. EC numbers are provided for each enzymatic step. O. oeni strains displaying metabolic blocks at individual enzymatic steps are also indicated. Arrows are color-coded according to the location of the ORF in parts B and C. B. A strain-specific genomic insertion predicted to impart the ability to utilise L-xylulose. Individual ORFs surrounding this locus are shown for each strain. Orthologous ORFs are positioned vertically and are color coded according to their conservation status (conserved, pink; strain-specific, light-blue). ORFs predicted to be directly involved in the utilisation of L-xylulose are color-coded according to their metabolic role (green, L-xylulose utilisation, orange, L-xylulose and L-arabinose utlisation). C. A strain-specific genomic insertion predicted to impart the ability to utilise arabinan and L-arabinose. Shading is identical to part B except for the presence of ORFs involved directly in the utilisation of arabinan and L-arabinose (shaded yellow).
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Figure 6: Variations in sugar utilisation pathways in O. oeni. A. The predicted pathway for the assimilation of L-arabinose and L-xylulose in O. oeni. EC numbers are provided for each enzymatic step. O. oeni strains displaying metabolic blocks at individual enzymatic steps are also indicated. Arrows are color-coded according to the location of the ORF in parts B and C. B. A strain-specific genomic insertion predicted to impart the ability to utilise L-xylulose. Individual ORFs surrounding this locus are shown for each strain. Orthologous ORFs are positioned vertically and are color coded according to their conservation status (conserved, pink; strain-specific, light-blue). ORFs predicted to be directly involved in the utilisation of L-xylulose are color-coded according to their metabolic role (green, L-xylulose utilisation, orange, L-xylulose and L-arabinose utlisation). C. A strain-specific genomic insertion predicted to impart the ability to utilise arabinan and L-arabinose. Shading is identical to part B except for the presence of ORFs involved directly in the utilisation of arabinan and L-arabinose (shaded yellow).

Mentions: In addition to intra-specific variation in the PTS transporter systems of O. oeni, there were also differences in metabolic pathways for sugar utilisation (Figure6). Arabinose and xylose are two sugars that have been noted as displaying strain-dependent utilisation profiles in O. oeni[33]. While genes imparting the ability to utilise xylose were not evident in the sequenced strains, the data supports strain-dependent metabolic potential to utilise L-arabinose (including the arabinose polymer arabinan) and L-xylulose (Figure6A).


Comparative analysis of the Oenococcus oeni pan genome reveals genetic diversity in industrially-relevant pathways.

Borneman AR, McCarthy JM, Chambers PJ, Bartowsky EJ - BMC Genomics (2012)

Variations in sugar utilisation pathways in O. oeni. A. The predicted pathway for the assimilation of L-arabinose and L-xylulose in O. oeni. EC numbers are provided for each enzymatic step. O. oeni strains displaying metabolic blocks at individual enzymatic steps are also indicated. Arrows are color-coded according to the location of the ORF in parts B and C. B. A strain-specific genomic insertion predicted to impart the ability to utilise L-xylulose. Individual ORFs surrounding this locus are shown for each strain. Orthologous ORFs are positioned vertically and are color coded according to their conservation status (conserved, pink; strain-specific, light-blue). ORFs predicted to be directly involved in the utilisation of L-xylulose are color-coded according to their metabolic role (green, L-xylulose utilisation, orange, L-xylulose and L-arabinose utlisation). C. A strain-specific genomic insertion predicted to impart the ability to utilise arabinan and L-arabinose. Shading is identical to part B except for the presence of ORFs involved directly in the utilisation of arabinan and L-arabinose (shaded yellow).
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Figure 6: Variations in sugar utilisation pathways in O. oeni. A. The predicted pathway for the assimilation of L-arabinose and L-xylulose in O. oeni. EC numbers are provided for each enzymatic step. O. oeni strains displaying metabolic blocks at individual enzymatic steps are also indicated. Arrows are color-coded according to the location of the ORF in parts B and C. B. A strain-specific genomic insertion predicted to impart the ability to utilise L-xylulose. Individual ORFs surrounding this locus are shown for each strain. Orthologous ORFs are positioned vertically and are color coded according to their conservation status (conserved, pink; strain-specific, light-blue). ORFs predicted to be directly involved in the utilisation of L-xylulose are color-coded according to their metabolic role (green, L-xylulose utilisation, orange, L-xylulose and L-arabinose utlisation). C. A strain-specific genomic insertion predicted to impart the ability to utilise arabinan and L-arabinose. Shading is identical to part B except for the presence of ORFs involved directly in the utilisation of arabinan and L-arabinose (shaded yellow).
Mentions: In addition to intra-specific variation in the PTS transporter systems of O. oeni, there were also differences in metabolic pathways for sugar utilisation (Figure6). Arabinose and xylose are two sugars that have been noted as displaying strain-dependent utilisation profiles in O. oeni[33]. While genes imparting the ability to utilise xylose were not evident in the sequenced strains, the data supports strain-dependent metabolic potential to utilise L-arabinose (including the arabinose polymer arabinan) and L-xylulose (Figure6A).

Bottom Line: These benefits are realised primarily through catalysing malolactic fermentation, but also through imparting other positive sensory properties.While any single strain of O. oeni was shown to contain around 1800 protein-coding genes, in-depth comparative annotation based on genomic synteny and protein orthology identified over 2800 orthologous open reading frames that comprise the pan genome of this species, and less than 1200 genes that make up the conserved genomic core present in all of the strains.This data is vital to understanding and harnessing the phenotypic variation present in this economically-important species.

View Article: PubMed Central - HTML - PubMed

Affiliation: The Australian Wine Research Institute, Glen Osmond, South Australia 5064, Australia. anthony.borneman@awri.com.au

ABSTRACT

Background: Oenococcus oeni, a member of the lactic acid bacteria, is one of a limited number of microorganisms that not only survive, but actively proliferate in wine. It is also unusual as, unlike the majority of bacteria present in wine, it is beneficial to wine quality rather than causing spoilage. These benefits are realised primarily through catalysing malolactic fermentation, but also through imparting other positive sensory properties. However, many of these industrially-important secondary attributes have been shown to be strain-dependent and their genetic basis it yet to be determined.

Results: In order to investigate the scale and scope of genetic variation in O. oeni, we have performed whole-genome sequencing on eleven strains of this bacterium, bringing the total number of strains for which genome sequences are available to fourteen. While any single strain of O. oeni was shown to contain around 1800 protein-coding genes, in-depth comparative annotation based on genomic synteny and protein orthology identified over 2800 orthologous open reading frames that comprise the pan genome of this species, and less than 1200 genes that make up the conserved genomic core present in all of the strains. The expansion of the pan genome relative to the coding potential of individual strains was shown to be due to the varied presence and location of multiple distinct bacteriophage sequences and also in various metabolic functions with potential impacts on the industrial performance of this species, including cell wall exopolysaccharide biosynthesis, sugar transport and utilisation and amino acid biosynthesis.

Conclusions: By providing a large cohort of sequenced strains, this study provides a broad insight into the genetic variation present within O. oeni. This data is vital to understanding and harnessing the phenotypic variation present in this economically-important species.

Show MeSH
Related in: MedlinePlus