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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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Variation in phosphotransferase (PTS) enzyme II systems in O. oeni. A. The occurrence and location of PTS enzyme II clusters across fourteen strains of O. oeni. The presence of a particular ORF in a specific strain is indicated (blue shading). Pseudogenes are also shown (grey shading). Individual PTS clusters are grouped by solid lines. B. A novel PTS IIC-glycosidase gene fusion in O. oeni strains AWRIB422 and AWRIB548. The two alternative genotypic arrangements are shown with areas of near complete sequence homology indicated by green shading. Genomic loci that display functional similarity (e.g. both proteins are PTS IIA subunits) are also indicated by pink shading.
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Figure 5: Variation in phosphotransferase (PTS) enzyme II systems in O. oeni. A. The occurrence and location of PTS enzyme II clusters across fourteen strains of O. oeni. The presence of a particular ORF in a specific strain is indicated (blue shading). Pseudogenes are also shown (grey shading). Individual PTS clusters are grouped by solid lines. B. A novel PTS IIC-glycosidase gene fusion in O. oeni strains AWRIB422 and AWRIB548. The two alternative genotypic arrangements are shown with areas of near complete sequence homology indicated by green shading. Genomic loci that display functional similarity (e.g. both proteins are PTS IIA subunits) are also indicated by pink shading.

Mentions: The range of sugars that O. oeni is capable of utilising is strain dependent [33]. To investigate the genetic basis of differences in sugar metabolism, we began by classifying genes that are predicted to encode phosphotransferase system (PTS) enzyme II sugar transporters in the O. oeni pan genome. In total, there were 46 PTS subunits that grouped into 18 separate genomic loci (individual subunits being adjacent in the genome) (Figure5). Fourteen of these loci contained either individual or multi-domain ORFs encoding IIA, IIB and IIC functions (and in two cases IID) in at least one strain and would therefore be expected to encode fully functional transporter complexes (Figure5). Correlating with differences in carbohydrate utilisation, only three of these complexes were conserved across all fourteen strains (in addition to three others in which strains contained potential pseudogenes in otherwise complete complexes).


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)

Variation in phosphotransferase (PTS) enzyme II systems in O. oeni. A. The occurrence and location of PTS enzyme II clusters across fourteen strains of O. oeni. The presence of a particular ORF in a specific strain is indicated (blue shading). Pseudogenes are also shown (grey shading). Individual PTS clusters are grouped by solid lines. B. A novel PTS IIC-glycosidase gene fusion in O. oeni strains AWRIB422 and AWRIB548. The two alternative genotypic arrangements are shown with areas of near complete sequence homology indicated by green shading. Genomic loci that display functional similarity (e.g. both proteins are PTS IIA subunits) are also indicated by pink shading.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3472311&req=5

Figure 5: Variation in phosphotransferase (PTS) enzyme II systems in O. oeni. A. The occurrence and location of PTS enzyme II clusters across fourteen strains of O. oeni. The presence of a particular ORF in a specific strain is indicated (blue shading). Pseudogenes are also shown (grey shading). Individual PTS clusters are grouped by solid lines. B. A novel PTS IIC-glycosidase gene fusion in O. oeni strains AWRIB422 and AWRIB548. The two alternative genotypic arrangements are shown with areas of near complete sequence homology indicated by green shading. Genomic loci that display functional similarity (e.g. both proteins are PTS IIA subunits) are also indicated by pink shading.
Mentions: The range of sugars that O. oeni is capable of utilising is strain dependent [33]. To investigate the genetic basis of differences in sugar metabolism, we began by classifying genes that are predicted to encode phosphotransferase system (PTS) enzyme II sugar transporters in the O. oeni pan genome. In total, there were 46 PTS subunits that grouped into 18 separate genomic loci (individual subunits being adjacent in the genome) (Figure5). Fourteen of these loci contained either individual or multi-domain ORFs encoding IIA, IIB and IIC functions (and in two cases IID) in at least one strain and would therefore be expected to encode fully functional transporter complexes (Figure5). Correlating with differences in carbohydrate utilisation, only three of these complexes were conserved across all fourteen strains (in addition to three others in which strains contained potential pseudogenes in otherwise complete complexes).

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