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Oenococcus Oeni Through Comparative Genomics of Apple Cider and Kombucha Strains

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Oenococcus Oeni Through Comparative Genomics of Apple Cider and Kombucha Strains Expanding the biodiversity of Oenococcus oeni through comparative genomics of apple cider and kombucha strains. Marc P. Lorentzen, Hugo Campbell-Sills, Tue S Jorgensen, Tue K Nielsen, Monika Coton, Emmanuel Coton, Lars Hansen, Patrick Lucas To cite this version: Marc P. Lorentzen, Hugo Campbell-Sills, Tue S Jorgensen, Tue K Nielsen, Monika Coton, et al.. Expanding the biodiversity of Oenococcus oeni through comparative genomics of apple cider and kombucha strains.. BMC Genomics, In press, 20 (1), pp.330. 10.1186/s12864-019-5692-3. hal- 03043113 HAL Id: hal-03043113 https://hal.archives-ouvertes.fr/hal-03043113 Submitted on 7 Dec 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Lorentzen et al. BMC Genomics (2019) 20:330 https://doi.org/10.1186/s12864-019-5692-3 RESEARCH ARTICLE Open Access Expanding the biodiversity of Oenococcus oeni through comparative genomics of apple cider and kombucha strains Marc P. Lorentzen1* , Hugo Campbell-Sills1,2, Tue S. Jorgensen3, Tue K. Nielsen3, Monika Coton4, Emmanuel Coton4, Lars Hansen3 and Patrick M. Lucas1 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. Keywords: Oenococcus oeni, Lactic acid bacteria, Comparative genomics, Phylogenomics, Pan-genome, Industrial microbiology Background domestication events, but also expand the toolbox of Oenococcus oeni is the main lactic acid bacteria (LAB) strain phenotypes that can be selected and used industri- species driving malolactic fermentation (MLF) in wine. ally [1, 2]. The species was first named “Leuconostoc The metabolic capabilities of O. oeni are of great interest oenos” on the basis of morphological and phenotypic due to its role in the wine industry, and by exploring its similarities with the members of the Leuconostoc genus. intraspecific biodiversity, we not only contribute to a However, it differs by its capacity to grow at low pH and better knowledge of the species and of potential is phylogenetically distant from other Leuconostoc spe- cies, which led to its reclassification in the Oenococcus genus in 1995 [3]. O. oeni is one of the three Oenococcus * Correspondence: [email protected] species described to date. The other two are O. kita- 1University of Bordeaux, ISVV, Unit Oenology, F-33882 Villenave d’Ornon, France harae, isolated from distillation residues of Japanese Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Lorentzen et al. BMC Genomics (2019) 20:330 Page 2 of 15 Shochu [4] and O. alcoholitolerans, collected from Bra- the two phylogroups A and B, whereas a consensus had zilian Cachaça and bioethanol plants [5]. not yet been reached regarding the existence of the third O. oeni is rarely detected in the natural environment, group C [12, 13]. MLST and phylogenomics have also even at the surface of grape berries in the vineyard [6]. revealed subgroups of strains that correlate with differ- In contrast, it is highly specialized to the wine environ- ent regions or product types such as cider, wine or ment thanks to its tolerance to low pH and high ethanol champagne [13, 31]. Recently, strains from two different levels. Although it is a minor species in grape must, it genetic subgroups were detected mainly in the Burgundy develops faster than all other LABs during and after al- and Champagne regions [11, 33]. They preferentially de- coholic fermentation and usually becomes the predom- velop in either red or white wine due to differences in inant bacterial species during MLF [7]. O. oeni was also their tolerance to low pH and phenolic compounds that frequently reported in French and Spanish apple cider differ between these two wine types [34]. where it also contributes to MLF [8, 9]. The genomic specialization of O. oeni contrasts with The first O. oeni genome sequence was released in other LAB species such as L. plantarum, the second 2005, from the strain PSU-1 [10]. This is a reference se- most abundant LAB species in wine, whose genomic quence not only because it was the first of this species, evolution appears to be detached from ecological con- but also because it is the only complete genome re- straints [35]. L. plantarum has a nomadic lifestyle, which ported to date, until this study. More recent studies have allowed it to acquire many genetic functions, but not to reported draft sequences of more than 200 strains ori- specialize to any specific environment. It is present in ginating from different wine types and regions [10–17]. many diverse environments, including wine, cider, kom- Like many other LAB species, O. oeni has a rather small bucha or shochu [36–38]. However, although it grows genome, ranging from 1.7 to 2.2 Mb, which most likely faster than O. oeni in culture media, it does not outcom- results from extensive loss of functions during pete O. oeni in the vast majority of wines. specialization of the species to life in wine, a The aim of this study was to clarify the population nutrient-rich environment [18]. The most striking fea- structure of O. oeni with the addition of new genomes ture of the O. oeni genome is that it lacks the mutS-- from strains isolated from cider that were not assigned mutL system involved in DNA mismatch repair. This to either A or B groups [33] and strains isolated from makes O. oeni a “hypermutable” species that accumu- kombucha, a fermented tea and an until recently un- lates spontaneous mutations 100 to 1000 times faster known niche of O. oeni [38]. The 9 cider strains were se- than other LAB species [19]. The full genome of strain lected on the basis of a genetic typing performed in a PSU-1 and genetic maps of 8 other strains showed that previous study which showed that they did not have the it contains only two sets of rRNA genes, whereas 4 to 9 characteristics of either group A or B strains [33] and are usually present in other LAB species [10, 20, 21]. the 5 kombucha strains were selected on the basis of The rRNA operon copy number probably correlates to PCR-M13 profiles [38]. Complete or draft genomes of the translational activity and growth kinetics of bacteria these strains were produced and analyzed along with all [22]. In agreement with this hypothesis, O. oeni is a fas- other O. oeni genomes reported to date in order to in- tidious and slow growing species compared to other vestigate their phylogenetic distribution and to identify LAB. The recent availability of numerous genome se- genes involved in adaptation to their environment of quences has made it possible to analyze the genomic isolation. variations in this species. Recently a pangenome assem- bly demonstrated variations in sugar and amino acid me- Results tabolism and the distribution of competence genes [12, De novo genome sequencing 14], and other studies have also reported genetic varia- To investigate O.
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