Expanding the biodiversity of Oenococcus oeni through comparative genomics of apple cider and kombucha strains

Abstract Background Oenococcus oeni is a lactic acid bacteria species adapted to the low pH, ethanol-rich environments of wine and cider fermentation, where it performs the crucial role of malolactic fermentation. It has a small genome and has lost the mutS-mutL DNA mismatch repair genes, making it...

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Published in:BMC Genomics
Main Authors: Marc P. Lorentzen, Hugo Campbell-Sills, Tue S. Jorgensen, Tue K. Nielsen, Monika Coton, Emmanuel Coton, Lars Hansen, Patrick M. Lucas
Format: Article
Language:English
Published: BMC 2019-05-01
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Online Access:http://link.springer.com/article/10.1186/s12864-019-5692-3
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author Marc P. Lorentzen
Hugo Campbell-Sills
Tue S. Jorgensen
Tue K. Nielsen
Monika Coton
Emmanuel Coton
Lars Hansen
Patrick M. Lucas
author_facet Marc P. Lorentzen
Hugo Campbell-Sills
Tue S. Jorgensen
Tue K. Nielsen
Monika Coton
Emmanuel Coton
Lars Hansen
Patrick M. Lucas
author_sort Marc P. Lorentzen
collection DOAJ
container_title BMC Genomics
description Abstract Background Oenococcus oeni is a lactic acid bacteria species adapted to the low pH, ethanol-rich environments of wine and cider fermentation, where it performs the crucial role of malolactic fermentation. It has a small genome and has lost the mutS-mutL DNA mismatch repair genes, making it a hypermutable and highly specialized species. Two main lineages of strains, named groups A and B, have been described to date, as well as other subgroups correlated to different types of wines or regions. A third group “C” has also been hypothesized based on sequence analysis, but it remains controversial. In this study we have elucidated the species population structure by sequencing 14 genomes of new strains isolated from cider and kombucha and performing comparative genomics analyses. Results Sequence-based phylogenetic trees confirmed a population structure of 4 clades: The previously identified A and B, a third group “C” consisting of the new cider strains and a small subgroup of wine strains previously attributed to group B, and a fourth group “D” exclusively represented by kombucha strains. A pair of complete genomes from group C and D were compared to the circularized O. oeni PSU-1 strain reference genome and no genomic rearrangements were found. Phylogenetic trees, K-means clustering and pangenome gene clusters evidenced the existence of smaller, specialized subgroups of strains. Using the pangenome, genomic differences in stress resistance and biosynthetic pathways were found to uniquely distinguish the C and D clades. Conclusions The obtained results, including the additional cider and kombucha strains, firmly established the O. oeni population structure. Group C does not appear as fully domesticated as group A to wine, but showed several unique patterns which may be due to ongoing specialization to the cider environment. Group D was shown to be the most divergent member of O. oeni to date, appearing as the closest to a pre-domestication state of the species.
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spelling doaj-art-3b41cfaa1aa04407bb5d43c1ffd7ca7a2025-08-19T20:10:06ZengBMCBMC Genomics1471-21642019-05-0120111510.1186/s12864-019-5692-3Expanding the biodiversity of Oenococcus oeni through comparative genomics of apple cider and kombucha strainsMarc P. Lorentzen0Hugo Campbell-Sills1Tue S. Jorgensen2Tue K. Nielsen3Monika Coton4Emmanuel Coton5Lars Hansen6Patrick M. Lucas7University of Bordeaux, ISVV, Unit OenologyUniversity of Bordeaux, ISVV, Unit OenologyDepartment of Environmental Science, Environmental Microbial Genomics Group, Aarhus UniversityDepartment of Environmental Science, Environmental Microbial Genomics Group, Aarhus UniversityUniversité de Brest, Laboratoire Universitaire de Biodiversité et Écologie Microbienne, EA 3882. ESIABUniversité de Brest, Laboratoire Universitaire de Biodiversité et Écologie Microbienne, EA 3882. ESIABDepartment of Environmental Science, Environmental Microbial Genomics Group, Aarhus UniversityUniversity of Bordeaux, ISVV, Unit OenologyAbstract Background Oenococcus oeni is a lactic acid bacteria species adapted to the low pH, ethanol-rich environments of wine and cider fermentation, where it performs the crucial role of malolactic fermentation. It has a small genome and has lost the mutS-mutL DNA mismatch repair genes, making it a hypermutable and highly specialized species. Two main lineages of strains, named groups A and B, have been described to date, as well as other subgroups correlated to different types of wines or regions. A third group “C” has also been hypothesized based on sequence analysis, but it remains controversial. In this study we have elucidated the species population structure by sequencing 14 genomes of new strains isolated from cider and kombucha and performing comparative genomics analyses. Results Sequence-based phylogenetic trees confirmed a population structure of 4 clades: The previously identified A and B, a third group “C” consisting of the new cider strains and a small subgroup of wine strains previously attributed to group B, and a fourth group “D” exclusively represented by kombucha strains. A pair of complete genomes from group C and D were compared to the circularized O. oeni PSU-1 strain reference genome and no genomic rearrangements were found. Phylogenetic trees, K-means clustering and pangenome gene clusters evidenced the existence of smaller, specialized subgroups of strains. Using the pangenome, genomic differences in stress resistance and biosynthetic pathways were found to uniquely distinguish the C and D clades. Conclusions The obtained results, including the additional cider and kombucha strains, firmly established the O. oeni population structure. Group C does not appear as fully domesticated as group A to wine, but showed several unique patterns which may be due to ongoing specialization to the cider environment. Group D was shown to be the most divergent member of O. oeni to date, appearing as the closest to a pre-domestication state of the species.http://link.springer.com/article/10.1186/s12864-019-5692-3Oenococcus oeniLactic acid bacteriaComparative genomicsPhylogenomicsPan-genomeIndustrial microbiology
spellingShingle Marc P. Lorentzen
Hugo Campbell-Sills
Tue S. Jorgensen
Tue K. Nielsen
Monika Coton
Emmanuel Coton
Lars Hansen
Patrick M. Lucas
Expanding the biodiversity of Oenococcus oeni through comparative genomics of apple cider and kombucha strains
Oenococcus oeni
Lactic acid bacteria
Comparative genomics
Phylogenomics
Pan-genome
Industrial microbiology
title Expanding the biodiversity of Oenococcus oeni through comparative genomics of apple cider and kombucha strains
title_full Expanding the biodiversity of Oenococcus oeni through comparative genomics of apple cider and kombucha strains
title_fullStr Expanding the biodiversity of Oenococcus oeni through comparative genomics of apple cider and kombucha strains
title_full_unstemmed Expanding the biodiversity of Oenococcus oeni through comparative genomics of apple cider and kombucha strains
title_short Expanding the biodiversity of Oenococcus oeni through comparative genomics of apple cider and kombucha strains
title_sort expanding the biodiversity of oenococcus oeni through comparative genomics of apple cider and kombucha strains
topic Oenococcus oeni
Lactic acid bacteria
Comparative genomics
Phylogenomics
Pan-genome
Industrial microbiology
url http://link.springer.com/article/10.1186/s12864-019-5692-3
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