Skip to main content
Log in

Mechanism analysis of combined acid-and-ethanol shock on Oenococcus oeni using RNA-Seq

  • Original Paper
  • Published:
European Food Research and Technology Aims and scope Submit manuscript

A Correction to this article was published on 13 August 2020

This article has been updated

Abstract

Acid-and-ethanol tolerance plays an important role in the cell viability of Oenococcus oeni and affects the enological characteristics of malolactic fermentation in wine. To reveal the mechanism of the response to acid-and-ethanol in O. oeni, we analyzed the changes to its gene expression profile after acid-and-ethanol shock for the first time using RNA-Seq. Some physiological indicators related to this stress response were also characterized. Bioinformatic and physiological analyses showed that the O. oeni strengthened the biosynthesis of peptidoglycan as a response to ethanol toxicity, and the cell membranes altered their fatty acid compositions for keeping the acidic H+ outside when the cells were shocked with acid-and-ethanol. When H+ entered the cytoplasm, the F0F1-ATPase system began discharging H+ (producing ATP), and the cells increased their expression of recN and mutT genes for minimizing the DNA damage. The cells also used two-component systems to communicate between same-species cells for improving the overall population survival rate. Genes encoding spermidine and putrescine transport were also upregulated to increase resistance to the acid-and-ethanol environment. This study fills important gaps in the current understanding of the bacterial acid-and-ethanol stress response mechanism, and it may be beneficial to screen more robust O. oeni strains in future works.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Change history

  • 13 August 2020

    In the original publication, there are errors in three sentence and reference number, the corrected presentation as follows.

References

  1. Guzzo J (2011) Stress responses of Oenococcus oeni. In: Tsakalidou E, Papadimitriou K (eds) Stress responses of lactic acid bacteria. Springer, Boston, pp 349–365

    Chapter  Google Scholar 

  2. Campbell-Sills H, Capozzi V, Romano A, Cappellin L, Spano G, Breniaux M, Lucas P, Biasioli F (2016) Advances in wine analysis by PTR-ToF-MS: Optimization of the method and discrimination of wines from different geographical origins and fermented with different malolactic starters. Int J Mass Spectrom 397–398:42–51

    Article  CAS  Google Scholar 

  3. Pérez-Martín F, Izquierdo-Cañas PM, Seseña S, García-Romero E, Palop ML (2015) Aromatic compounds released from natural precursors by selected Oenococcus oeni strains during malolactic fermentation. Eur Food Res Technol 240(3):609–618

    Article  CAS  Google Scholar 

  4. Henríquez-Aedo K, Durán D, Garcia A, Hengst MB, Aranda M (2016) Identification of biogenic amines-producing lactic acid bacteria isolated from spontaneous malolactic fermentation of chilean red wines. LWT - Food Sci Technol 68:183–189

    Article  CAS  Google Scholar 

  5. López I, Tenorio C, Zarazaga M, Dizy M, Torres C, Ruiz-Larrea F (2007) Evidence of mixed wild populations of Oenococcus oeni strains during wine spontaneous malolactic fermentations. Eur Food Res Technol 226(1):215–223

    Article  CAS  Google Scholar 

  6. Berbegal C, Peña N, Russo P, Grieco F, Pardo I, Ferrer S, Spano G, Capozzi V (2016) Technological properties of Lactobacillus plantarum strains isolated from grape must fermentation. Food Microbiol 57:187–194

    Article  CAS  PubMed  Google Scholar 

  7. Genisheva Z, Mota A, Mussatto SI, Oliveira JM, Teixeira JA (2014) Integrated continuous winemaking process involving sequential alcoholic and malolactic fermentations with immobilized cells. Process Biochem 49(1):1–9

    Article  CAS  Google Scholar 

  8. Brizuela NS, Bravo-Ferrada BM, Pozo-Bayon MA, Semorile L, Elizabeth Tymczyszyn E (2018) Changes in the volatile profile of Pinot noir wines caused by Patagonian Lactobacillus plantarum and Oenococcus oeni strains. Food Res Int 106:22–28

    Article  CAS  PubMed  Google Scholar 

  9. Cinquanta L, De Stefano G, Formato D, Niro S, Panfili G (2018) Effect of pH on malolactic fermentation in southern Italian wines. Eur Food Res Technol 244(7):1261–1268

    Article  CAS  Google Scholar 

  10. Bartowsky EJ, Henschke PA (2008) Acetic acid bacteria spoilage of bottled red wine – a review. Int J Food Microbiol 125(1):60–70

    Article  CAS  PubMed  Google Scholar 

  11. Lonvaud-Funel A (2001) Biogenic amines in wines: role of lactic acid bacteria. FEMS Microbiol Lett 199(1):9–13

    Article  CAS  PubMed  Google Scholar 

  12. Margalef-Catala M, Felis GE, Reguant C, Stefanelli E, Torriani S, Bordons A (2017) Identification of variable genomic regions related to stress response in Oenococcus oeni. Food Res Int 102:625–638

    Article  CAS  PubMed  Google Scholar 

  13. Margalef-Catala M, Stefanelli E, Araque I, Wagner K, Felis GE, Bordons A, Torriani S, Reguant C (2017) Variability in gene content and expression of the thioredoxin system in Oenococcus oeni. Food Microbiol 61:23–32

    Article  CAS  PubMed  Google Scholar 

  14. Maitre M, Weidmann S, Dubois-Brissonnet F, David V, Covès J, Guzzo J (2014) Adaptation of the wine bacterium Oenococcus oeni to ethanol stress: role of the small heat shock protein Lo18 in membrane integrity. Appl Environ Microb 80(10):2973

    Article  CAS  Google Scholar 

  15. Bonomo MG, Cafaro C, Guerrieri A, Crispo F, Milella L, Calabrone L, Salzano G (2017) Flow cytometry and capillary electrophoresis analyses in ethanol-stressed Oenococcus oeni strains and changes assessment of membrane fatty acid composition. J Appl Microbiol 122(6):1615–1626

    Article  CAS  PubMed  Google Scholar 

  16. Margalef-Catala M, Araque I, Weidmann S, Guzzo J, Bordons A, Reguant C (2016) Protective role of glutathione addition against wine-related stress in Oenococcus oeni. Food Res Int 90:8–15

    Article  CAS  PubMed  Google Scholar 

  17. Olguin N, Bordons A, Reguant C (2010) Multigenic expression analysis as an approach to understanding the behaviour of Oenococcus oeni in wine-like conditions. Int J Food Microbiol 144(1):88–95

    Article  CAS  PubMed  Google Scholar 

  18. Fu X, Li P, Zhang L, Li S (2018) RNA-Seq-based transcriptomic analysis of Saccharomyces cerevisiae during solid-state fermentation of crushed sweet sorghum stalks. Process Biochem 68:53–63

    Article  CAS  Google Scholar 

  19. Pan L, Chen X, Wang K, Mao Z (2019) A temporal transcriptomic dynamics study reveals the reason of enhanced ε-poly-L-lysine production in Streptomyces albulus M-Z18 by pH shock. Process Biochem 85:1–11

    Article  CAS  Google Scholar 

  20. Liu L, Zhao H, Peng S, Wang T, Su J, Liang Y, Li H, Wang H (2017) Transcriptomic analysis of Oenococcus oeni SD-2a response to acid shock by RNA-Seq. Front Microbiol 8:1586

    Article  PubMed  PubMed Central  Google Scholar 

  21. Sternes PR, Costello PJ, Chambers PJ, Bartowsky EJ, Borneman AR (2017) Whole transcriptome RNAseq analysis of Oenococcus oeni reveals distinct intra-specific expression patterns during malolactic fermentation, including genes involved in diacetyl metabolism. Int J Food Microbiol 257:216–224

    Article  CAS  PubMed  Google Scholar 

  22. Li H, Wang A, Li Z, Zhao W, Wang H (2009) Influence of acid stress on the viability and its relationship to the induction of stress protein of Oenococcus oeni SD-2a. Agr Sci China 8:311–316

    Article  CAS  Google Scholar 

  23. Margalef-Català M, Araque I, Bordons A, Reguant C, Bautista-Gallego J (2016) Transcriptomic and proteomic analysis of Oenococcus oeni adaptation to wine stress conditions. Front Microbiol 7:1554

    Article  PubMed  PubMed Central  Google Scholar 

  24. Parreira VR, Russell K, Athanasiadou S, Prescott JF (2016) Comparative transcriptome analysis by RNAseq of necrotic enteritis Clostridium perfringens during in vivo colonization and in vitro conditions. BMC Microbiol 16(1):186

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Olguín N, Bordons A, Reguant C (2009) Influence of ethanol and pH on the gene expression of the citrate pathway in Oenococcus oeni. Food Microbiol 26(2):197–203

    Article  PubMed  CAS  Google Scholar 

  26. Peng S, Liu L, Zhao H, Wang H, Li H (2018) Selection and validation of reference genes for quantitative real-time PCR normalization under ethanol stress conditions in Oenococcus oeni SD-2a. Front Microbiol 9:892

    Article  PubMed  PubMed Central  Google Scholar 

  27. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25(4):402–408

    Article  CAS  PubMed  Google Scholar 

  28. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem and Physiol 37(8):911–917

    Article  CAS  Google Scholar 

  29. López CS, Heras H, Ruzal SM, Sánchez-Rivas C, Rivas EA (1998) Variations of the envelope composition of Bacillus subtilis during growth in hyperosmotic medium. Curr Microbiol 36(1):55–61

    Article  PubMed  Google Scholar 

  30. Garbay S, Rozes N, Lonvaud-Funel A (1995) Fatty acid composition of Leuconostoc oenos, incidence of growth conditions and relationship with malolactic efficiency. Food Microbiol 12:387–395

    Article  CAS  Google Scholar 

  31. Liu S, Ren F, Jiang J, Zhao L (2016) Acid response of Bifidobacterium longum subsp. longum BBMN68 is accompanied by modification of the cell membrane fatty acid composition. J Microbiol Biotechnol 26(7):1190–1197

    Article  CAS  PubMed  Google Scholar 

  32. Zhao H, Liu L, Peng S, Yuan L, Li H, Wang H (2019) Heterologous expression of argininosuccinate synthase from Oenococcus oeni enhances the acid resistance of Lactobacillus plantarum. Front Microbiol 10:1393

    Article  PubMed  PubMed Central  Google Scholar 

  33. Ultee E, Ramijan K, Dame R T, Briegel A, Claessen D (2019) Chapter Two-Stress induced adaptive morphogenesis in bacteria. In: Poole RK (eds.) Advances in Microbial Physiology. Academic Press, pp 97–141.

  34. Bonomo M, Di Tomaso K, Calabrone L, Salzano G (2018) Ethanol stress in Oenococcus oeni: Transcriptional response and complex physiological mechanisms. J Appl Microbiol 125:2–15

    Article  CAS  PubMed  Google Scholar 

  35. To TMH, Grandvalet C, Tourdot-Maréchal R (2011) Cyclopropanation of membrane unsaturated fatty acids is not essential to the acid stress response of Lactococcus lactis subsp. cremoris. Appl Environ Microb 77(10):3327–3334

    Article  CAS  Google Scholar 

  36. Fortier LC, Tourdot-Marechal R, Divies C, Lee BH, Guzzo J (2003) Induction of Oenococcus oeni H+-ATPase activity and mRNA transcription under acidic conditions. FEMS Microbiol Lett 222(2):165–169

    Article  CAS  PubMed  Google Scholar 

  37. Nygaard P, Duckert P, Saxild HH (1996) Role of adenine deaminase in purine salvage and nitrogen metabolism and characterization of the ade gene in Bacillus subtilis. J Bacteriol 178(3):846–853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Jin J, Zhang B, Guo H, Cui J, Jiang L, Song S, Sun M, Ren F (2012) Mechanism analysis of acid tolerance response of Bifidobacterium longum subsp longum BBMN 68 by gene expression profile using RNA-sequencing. PLoS ONE 7(12):e50777–e50777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Wu C, Zhang J, Wang M, Du G, Chen J (2012) Lactobacillus casei combats acid stress by maintaining cell membrane functionality. J Ind Microbiol Biot 39(7):1031–1039

    Article  CAS  Google Scholar 

  40. Li Z, Nair SK (2012) Quorum sensing: how bacteria can coordinate activity and synchronize their response to external signals? Protein sci 21(10):1403–1417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Rutherford ST, Bassler BL (2012) Bacterial quorum sensing: its role in virulence and possibilities for its control. CSH Perspect Med 2:11

    Google Scholar 

  42. Senadheera D, Krastel K, Mair R, Persadmehr A, Abranches J, Burne RA, Cvitkovitch DG (2009) Inactivation of VicK affects acid production and acid survival of Streptococcus mutans. J Bacteriol 191(20):6415–6424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Cox DJ, Henickkling T (1995) Protonmotive force and atp generation during malolactic fermentation. Am J Enol Viticult 46(3):319–323

    CAS  Google Scholar 

  44. Augagneur Y, Ritt J-F, Linares DM, Remize F, Tourdot-Maréchal R, Garmyn D, Guzzo J (2007) Dual effect of organic acids as a function of external pH in Oenococcus oeni. Arch Microbiol 188(2):147–157

    Article  CAS  PubMed  Google Scholar 

  45. Kashiwagi K, Igarashi K (2011) Identification and assays of polyamine transport systems in Escherichia coli and Saccharomyces cerevisiae. In: Pegg AE, Casero JRA (eds) Polyamines: methods and protocols. Humana Press, Totowa, pp 295–308

    Chapter  Google Scholar 

  46. Olguin N, Champomier-Verges M, Anglade P, Baraige F, Cordero-Otero R, Bordons A, Zagorec M, Reguant C (2015) Transcriptomic and proteomic analysis of Oenococcus oeni PSU-1 response to ethanol shock. Food Microbiol 51:87–95

    Article  CAS  PubMed  Google Scholar 

  47. Igarashi K, Kashiwagi K (2000) Polyamines: Mysterious Modulators of Cellular Functions. Biochem Bioph Res Co 271(3):559–564

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant No. 31471708). We thank China Association for Science and Technology (CAST).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Hua Li or Hua Wang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Compliance with ethics requirements

This article does not contain any studies with human or animal subjects.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 214 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, H., Liu, L., Yuan, L. et al. Mechanism analysis of combined acid-and-ethanol shock on Oenococcus oeni using RNA-Seq. Eur Food Res Technol 246, 1637–1646 (2020). https://doi.org/10.1007/s00217-020-03520-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00217-020-03520-0

Keywords

Navigation