Comparative genomic analysis of 255 Oenococcus oeni isolates from China: unveiling strain diversity and genotype-phenotype associations of acid resistance

ABSTRACT Oenococcus oeni, the only species of lactic acid bacteria capable of fully completing malolactic fermentation under challenging wine conditions, continues to intrigue researchers owing to its remarkable adaptability, particularly in combating acid stress. However, the mechanism underlying i...

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التفاصيل البيبلوغرافية
الحاوية / القاعدة:Microbiology Spectrum
المؤلفون الرئيسيون: Wei Chi, Hanwen Zhang, Xinyi Li, Yeqin Zhou, Qiang Meng, Ling He, Yafan Yang, Shuwen Liu, Kan Shi
التنسيق: مقال
اللغة:الإنجليزية
منشور في: American Society for Microbiology 2025-06-01
الموضوعات:
الوصول للمادة أونلاين:https://journals.asm.org/doi/10.1128/spectrum.03265-24
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author Wei Chi
Hanwen Zhang
Xinyi Li
Yeqin Zhou
Qiang Meng
Ling He
Yafan Yang
Shuwen Liu
Kan Shi
author_facet Wei Chi
Hanwen Zhang
Xinyi Li
Yeqin Zhou
Qiang Meng
Ling He
Yafan Yang
Shuwen Liu
Kan Shi
author_sort Wei Chi
collection DOAJ
container_title Microbiology Spectrum
description ABSTRACT Oenococcus oeni, the only species of lactic acid bacteria capable of fully completing malolactic fermentation under challenging wine conditions, continues to intrigue researchers owing to its remarkable adaptability, particularly in combating acid stress. However, the mechanism underlying its superior adaptation to wine stresses still remains elusive due to the lack of viable genetic manipulation tools for this species. In this study, we conducted genomic sequencing and acid resistance phenotype analysis of 255 O. oeni isolates derived from diverse wine regions across China, aiming to elucidate their strain diversity and genotype-phenotype associations of acid resistance through comparative genomics. A significant correlation between phenotypes and evolutionary relationships was observed. Notably, phylogroup B predominantly consisted of acid-resistant isolates, primarily originating from Shandong and Shaanxi wine regions. Furthermore, we uncovered a noteworthy linkage between prophage genomic islands and acid resistance phenotype. Using genome-wide association studies, we identified key genes correlated with acid resistance, primarily involved in carbohydrates and amino acid metabolism processes. This study offers profound insights into the genetic diversity and genetic basis underlying adaptation mechanisms to acid stress in O. oeni.IMPORTANCEThis study provides valuable insights into the genetic basis of acid resistance in Oenococcus oeni, a key lactic acid bacterium in winemaking. By analyzing 255 isolates from diverse wine regions in China, we identified significant correlations between strain diversity, genomic islands, and acid resistance phenotypes. Our findings reveal that certain prophage-related genomic islands and specific genes are closely linked to acid resistance, offering a deeper understanding of how O. oeni adapts to acidic environments. These discoveries not only advance our knowledge of microbial stress responses but also pave the way for selecting and engineering acid-resistant strains, enhancing malolactic fermentation efficiency and wine quality. This research underscores the importance of genomics in improving winemaking practices and addressing challenges posed by high-acidity wines.
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spelling doaj-art-16f9f17c8dd04403bfec1188fefb4ad42025-08-20T02:05:24ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972025-06-0113610.1128/spectrum.03265-24Comparative genomic analysis of 255 Oenococcus oeni isolates from China: unveiling strain diversity and genotype-phenotype associations of acid resistanceWei Chi0Hanwen Zhang1Xinyi Li2Yeqin Zhou3Qiang Meng4Ling He5Yafan Yang6Shuwen Liu7Kan Shi8College of Enology, College of Horticulture, Shaanxi Engineering Research Center for Viti-Viniculture, Viti-Viniculture Engineering Technology Center of State Forestry and Grassland Administration, Heyang Experimental and Demonstrational Stations for Grape, Ningxia Helan Mountain's East Foothill Wine Experiment and Demonstration Station, Northwest A&F University, Yangling, Shaanxi, ChinaCollege of Enology, College of Horticulture, Shaanxi Engineering Research Center for Viti-Viniculture, Viti-Viniculture Engineering Technology Center of State Forestry and Grassland Administration, Heyang Experimental and Demonstrational Stations for Grape, Ningxia Helan Mountain's East Foothill Wine Experiment and Demonstration Station, Northwest A&F University, Yangling, Shaanxi, ChinaCollege of Enology, College of Horticulture, Shaanxi Engineering Research Center for Viti-Viniculture, Viti-Viniculture Engineering Technology Center of State Forestry and Grassland Administration, Heyang Experimental and Demonstrational Stations for Grape, Ningxia Helan Mountain's East Foothill Wine Experiment and Demonstration Station, Northwest A&F University, Yangling, Shaanxi, ChinaCollege of Enology, College of Horticulture, Shaanxi Engineering Research Center for Viti-Viniculture, Viti-Viniculture Engineering Technology Center of State Forestry and Grassland Administration, Heyang Experimental and Demonstrational Stations for Grape, Ningxia Helan Mountain's East Foothill Wine Experiment and Demonstration Station, Northwest A&F University, Yangling, Shaanxi, ChinaCollege of Food Science and Technology, Northwest University, Xi’an, Shaanxi, ChinaCollege of Enology, College of Horticulture, Shaanxi Engineering Research Center for Viti-Viniculture, Viti-Viniculture Engineering Technology Center of State Forestry and Grassland Administration, Heyang Experimental and Demonstrational Stations for Grape, Ningxia Helan Mountain's East Foothill Wine Experiment and Demonstration Station, Northwest A&F University, Yangling, Shaanxi, ChinaCollege of Enology, College of Horticulture, Shaanxi Engineering Research Center for Viti-Viniculture, Viti-Viniculture Engineering Technology Center of State Forestry and Grassland Administration, Heyang Experimental and Demonstrational Stations for Grape, Ningxia Helan Mountain's East Foothill Wine Experiment and Demonstration Station, Northwest A&F University, Yangling, Shaanxi, ChinaCollege of Enology, College of Horticulture, Shaanxi Engineering Research Center for Viti-Viniculture, Viti-Viniculture Engineering Technology Center of State Forestry and Grassland Administration, Heyang Experimental and Demonstrational Stations for Grape, Ningxia Helan Mountain's East Foothill Wine Experiment and Demonstration Station, Northwest A&F University, Yangling, Shaanxi, ChinaCollege of Enology, College of Horticulture, Shaanxi Engineering Research Center for Viti-Viniculture, Viti-Viniculture Engineering Technology Center of State Forestry and Grassland Administration, Heyang Experimental and Demonstrational Stations for Grape, Ningxia Helan Mountain's East Foothill Wine Experiment and Demonstration Station, Northwest A&F University, Yangling, Shaanxi, ChinaABSTRACT Oenococcus oeni, the only species of lactic acid bacteria capable of fully completing malolactic fermentation under challenging wine conditions, continues to intrigue researchers owing to its remarkable adaptability, particularly in combating acid stress. However, the mechanism underlying its superior adaptation to wine stresses still remains elusive due to the lack of viable genetic manipulation tools for this species. In this study, we conducted genomic sequencing and acid resistance phenotype analysis of 255 O. oeni isolates derived from diverse wine regions across China, aiming to elucidate their strain diversity and genotype-phenotype associations of acid resistance through comparative genomics. A significant correlation between phenotypes and evolutionary relationships was observed. Notably, phylogroup B predominantly consisted of acid-resistant isolates, primarily originating from Shandong and Shaanxi wine regions. Furthermore, we uncovered a noteworthy linkage between prophage genomic islands and acid resistance phenotype. Using genome-wide association studies, we identified key genes correlated with acid resistance, primarily involved in carbohydrates and amino acid metabolism processes. This study offers profound insights into the genetic diversity and genetic basis underlying adaptation mechanisms to acid stress in O. oeni.IMPORTANCEThis study provides valuable insights into the genetic basis of acid resistance in Oenococcus oeni, a key lactic acid bacterium in winemaking. By analyzing 255 isolates from diverse wine regions in China, we identified significant correlations between strain diversity, genomic islands, and acid resistance phenotypes. Our findings reveal that certain prophage-related genomic islands and specific genes are closely linked to acid resistance, offering a deeper understanding of how O. oeni adapts to acidic environments. These discoveries not only advance our knowledge of microbial stress responses but also pave the way for selecting and engineering acid-resistant strains, enhancing malolactic fermentation efficiency and wine quality. This research underscores the importance of genomics in improving winemaking practices and addressing challenges posed by high-acidity wines.https://journals.asm.org/doi/10.1128/spectrum.03265-24lactic acid bacteriapan-genomegenomic islandhorizontal gene transfergenome-wide association study
spellingShingle Wei Chi
Hanwen Zhang
Xinyi Li
Yeqin Zhou
Qiang Meng
Ling He
Yafan Yang
Shuwen Liu
Kan Shi
Comparative genomic analysis of 255 Oenococcus oeni isolates from China: unveiling strain diversity and genotype-phenotype associations of acid resistance
lactic acid bacteria
pan-genome
genomic island
horizontal gene transfer
genome-wide association study
title Comparative genomic analysis of 255 Oenococcus oeni isolates from China: unveiling strain diversity and genotype-phenotype associations of acid resistance
title_full Comparative genomic analysis of 255 Oenococcus oeni isolates from China: unveiling strain diversity and genotype-phenotype associations of acid resistance
title_fullStr Comparative genomic analysis of 255 Oenococcus oeni isolates from China: unveiling strain diversity and genotype-phenotype associations of acid resistance
title_full_unstemmed Comparative genomic analysis of 255 Oenococcus oeni isolates from China: unveiling strain diversity and genotype-phenotype associations of acid resistance
title_short Comparative genomic analysis of 255 Oenococcus oeni isolates from China: unveiling strain diversity and genotype-phenotype associations of acid resistance
title_sort comparative genomic analysis of 255 oenococcus oeni isolates from china unveiling strain diversity and genotype phenotype associations of acid resistance
topic lactic acid bacteria
pan-genome
genomic island
horizontal gene transfer
genome-wide association study
url https://journals.asm.org/doi/10.1128/spectrum.03265-24
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