Preferences help
enabled [disable] Abstract
Number of results
2017 | 64 | 3 | 459-464
Article title

Lactic acid bacteria stress response to preservation processes in the beverage and juice industry

Title variants
Languages of publication
In this review we summarize stress factors that affect the lactic acid bacteria (LAB) and cause different molecular stress responses. LAB belong to a group of bacteria that is very widespread in food and beverages. They are present, and desired, in fermented products like yogurts, cheese, vegetables, meat or wine. In most of them, LAB are providing positive sensory and nutritive features. However, as harmless and desired microbes in one product, LAB can cause spoilage and a bad taste of others, especially in juices and beverages. LAB are resistant to many stress factors which allows them to survive in harsh environments. The most common stress factors they have to deal with are: heat, cold, acidity, NaCl and high hydrostatic pressure (HHP). Their ability to survive depends on their skills to cope with stress factors. Under stress conditions, LAB activate mechanisms that allow them to adjust to the new conditions, which can influence their viability and technological properties. This ability to adapt to different stress conditions may come from the cross-protection systems they have, as resistance to one factor may help them to deal with the other stress effectors. LAB are highly valuable for the food industry and that is why it is important to understand their stress response mechanisms.
Physical description
  • Department of Fruit and Vegetable Products Technology, prof. Wacław Dąbrowski Institute of Agricultural and Food Biotechnology, Warsaw, Poland
  • Department of Fruit and Vegetable Products Technology, prof. Wacław Dąbrowski Institute of Agricultural and Food Biotechnology, Warsaw, Poland
  • Alegría EG, López I, Ruiz JI, Saenz J, Fernández E, Zarazaga M, Dizy M, Torres C, Ruiz-Larrea F (2004) High tolerance of wild Lactobacillus plantarum and Oenococcus oeni strains to lyophilisation and stress environmental conditions of acid pH and ethanol. FEMS Microbiol Lett 230: 53-61. doi: 10.1016/S0378-1097(03)00854-1.
  • Ananta E, Knorr D (2004) Evidence on the role of protein biosynthesis in the induction of heat tolerance of Lactobacillus rhamnosus GG by pressure pre-treatment. Int J Food Microbiol 96: 307-313. doi: 10.1016/j.ijfoodmicro.2004.04.012.
  • Asano S, Suzuki K, Iijima K, Motoyama H, Kuriyama H, Kitagawa Y (2007) Effects of morphological changes in beer-spoilage lactic acid bacteria on membrane filtration in breweries. J Biosci Bioeng 104: 334-338. doi: 10.1263/jbb.104.334.
  • Back W (2005) Colour Atlas and Handbook of Beverage Biology. Back ed. pp 317. Verlag Hans Carl: Nürnberg, Germany
  • Blaiotta G, Fusco V, Ercolini D, Aponte M, Pepe O, Villani F (2008) Lactobacillus strain diversity based on partial hsp60 gene sequences and design of PCR restriction fragment length polymorphism assays for species identification and differentiation. Appl Environ Microbiol 74: 208-215. doi: 10.1128/AEM.01711-07.
  • Bron PA, Molenaar D, de Vos WM, Kleerebezem M (2006) DNA micro-array-based identification of bile-responsive genes in Lactobacillus plantarum. J Appl Microbiol 100: 728-738. doi: 10.4161/bbug.2.2.13910.
  • Castaldo C, Siciliano RA, Muscariello L, Marasco R, Sacco M (2006) CcpA affects expression of the groESL and dnaK operons in Lactobacillus plantarum. Microbial Cell Factories 5: 35. doi: 10.1186/1475-2859-5-35.
  • Chastanet A, Fert J, Msadek T (2003) Comparative genomics reveal novel heat shock regulatory mechanisms in Staphylococcus aureus and other Gram-positive bacteria. Mol Microbiol 47: 1061-1073. doi: 10.1046/j.1365-2958.2003.03355.x.
  • Chastanet A, Msadek T (2003) ClpP of Streptococcus salivarius is a novel member of the dually regulated class of stress response genes in gram-positive bacteria. J Bacteriol 185: 683-687. doi: 10.1128/JB.185.2.683-687.2003.
  • Chung HJ, Bang W, Drake M (2006) Stress response of Escherichia coli. Comp Rev Food Sci Food Safety 5: 52-64. doi: 10.1111/j.1541-4337.2006.00002.x
  • Considine KM, Kelly AL, Fitzgerald GF, Hill C, Sleator RD (2008) High-pressure processing--effects on microbial food safety and food quality. FEMS Microbiol Lett 281: 1-9. doi: 10.1111/j.1574-6968.2008.01084.x.
  • Darmon E, Noone D, Masson A, Bron S, Kuipers OP, Devine KM, van Dijl JM (2002) A novel class of heat and secretion stress-responsive genes is controlled by the autoregulated CssRS two-component system of Bacillus subtilis. J Bacteriol 184: 5661-5671. doi: 10.1128/JB.184.20.5661-5671.2002.
  • De Angelis M, Di Cagno R, Huet C, Crecchio C, Fox PF, Gobbetti M (2004) Heat shock response in Lactobacillus plantarum. Appl Environ Microbiol 70: 1336-1346. doi: 10.1128/AEM.70.3.1336-1346.2004.
  • De Angelis M., Gobbetti M (2011) Stress responses of lactobacilli. In Stress responses of lactic acid bacteria, Papadimitriou K, Tsakalidou E eds, pp 219-249. Springer, New York. doi: 10.1007/978-0-387-92771-8.
  • Derré I, Rapoport G, Msadek T (1999) CtsR, a novel regulator of stress and heat shock response, controls clp and molecular chaperone gene expression in Gram-positive bacteria. Mol Microbiol 31: 117-131. doi: 10.1046/j.1365-2958.1999.01152.x.
  • Derré I, Rapoport G, Msadek T (2000) The CtsR regulator of stress response is active as a dimer and specifically degraded in vivo at 37°C. Mol Microbiol 38: 335-347. doi: 10.1046/j.1365-2958.2000.02124.x.
  • Derré I, Rapoport G, Devine K, Rose M, Msadek T (1999) ClpE, a novel type of HSP100 ATPase, is part of the CtsR heat shock regulon of Bacillus subtilis. Mol Microbiol 32: 581-593. doi: 10.1046/j.1365-2958.1999.01374.x.
  • Di Cagno R, Minervini G, Sgarbi E, Lazzi C, Bernini V, Neviani E, Gobbetti M (2010) Comparison of phenotypic (Biolog System) and genotypic (random amplified polymorphic DNA-polymerase chain reaction, RAPD-PCR, and amplified fragment length polymorphism, AFLP) methods for typing Lactobacillus plantarum isolates from raw vegetables and fruits. Int J Food Microbiol 143: 246-253. doi: 10.1016/j.ijfoodmicro.2010.08.018.
  • Drews O, Weiss W, Reil G, Parlar H, Wait R, Görg A (2002) High pressure effects step-wise altered protein expression in Lactobacillus sanfranciscensis. Proteomics 2: 765-774. doi: 10.1002/1615-9861(200206)2:6<765::AID-PROT765>3.0.CO;2-V.
  • Ehrmann MA, Scheyhing CH, Vogel RF (2001) In vitro stability and expression of green fluorescent protein under high pressure conditions. Lett Appl Microbiol 32: 230-234. doi: 10.1046/j.1472-765X.2001.00892.x.
  • Fiocco D, Collins M, Muscariello L, Hols P, Kleerebezem M, Msadek T, Spano G (2009) The Lactobacillus plantarum ftsH gene is a novel member of the CtsR stress response regulon. J Bacteriol 191: 1688-1694. doi: 10.1128/JB.01551-08.
  • Fiocco D, Capozzi V, Collins M., Gallone A, Hols P, Guzzo J, Weidmann S, Rieu A, Msadek T, Spano G (2010) Characterization of the CtsR stress response regulon in Lactobacillus plantarum. J Bacteriol 192: 896-900. doi: 10.1128/JB.01122-09.
  • Franz CMAP and Holzapfel WH. (2011) Chapter 1. The Importance of Understanding the Stress Physiology of Lactic Acid Bacteria. In Stress responses of lactic acid bacteria, Papadimitrious K, Tsakalidou E eds, 530: 13-15. Springer Science & Business Media. doi: 10.1007/978-0-387-92771-8.
  • Garai-Ibabe G, Ibarburu I, Berregi I, Claisse O, Lonvaud-Funel A, Irastorza A, Dueñas MT (2008) Glycerol metabolism and bitterness producing lactic acid bacteria in cidermaking. Int J Food Microbiol 121: 253-261. doi: 10.1016/j.ijfoodmicro.2007.11.004.
  • Gökmen V, Acar J (2004) Fumaric acid in apple juice: a potential indicator of microbial spoilage of apples used as raw material. Food Addit Contam 21: 626-631. doi: 10.1080/02652030410001712501.
  • Guidone A, Parente E, Zotta T, Guinane CM, Rea MC, Stanton C, Ross RP, Ricciardi A (2015) Polymorphisms in stress response genes in Lactobacillus plantarum: implications for classification and heat stress response. Ann Microbiology 65: 297-305. doi: 10.1007/s13213-014-0862-7
  • Hammes W, Hertel C (2009) Genus I. Lactobacillus beijerinck 1901, 212AL. In Bergey's Manual of Systematic Bacteriology, De Vos P, Garrity G, Jones D, Krieg NR, Ludwig W, Rainey FA, Schleifer KH, Whitman WB eds, 2nd edn, pp 465-513. New York, Springer. doi: 10.1007/0-387-28022-7.
  • Hecker M, Schumann W, Volker U (1996) Heat-shock and general stress response in Bacillus subtilis. Mol Microbiol 19: 417-428. doi: 10.1046/j.1365-2958.1996.396932.x.
  • Helmann JD, Wu MF, Kobel PA, Gamo FJ, Wilson M., Morshedi MM, Navre M, Paddon C. (2001) Global transcriptional response of Bacillus subtilis to heat shock. J Bacteriol 183: 7318-7328. doi: 10.1128/JB.183.24.7318-7328.2001.
  • Hörmann S, Scheyhing C, Behr J, Pavlovic M, Ehrmann M, Vogel RF (2006) Comparative proteome approach to characterize the high-pressure stress response of Lactobacillus sanfranciscensis DSM 20451(T). Proteomics 6: 1878-1885. doi: 10.1002/pmic.200402086.
  • Huang CC, Lee FL, Liou JS (2010) Rapid discrimination and classification of the Lactobacillus plantarum group based on a partial dnaK sequence and DNA fingerprinting techniques. Antonie Van Leeuwenhoek 97: 289-296. doi: 10.1007/s10482-009-9409-5.
  • Ibarburu I, Aznar R, Elizaquível P, García-Quintáns N, Lopéz P, Munduate A, Irastorza A, Dueñas MT (2010) A real-time PCR assay for detection and quatification of 2-branched (1,3)-D-glucan producing lactic acid bacteria in cider. Int J Food Microbiol 143: 26-31. doi: 10.1016/j.ijfoodmicro.2010.07.023.
  • Ingmer H, Vogensen FK, Hammer K, Kilstrup M (1999) Disruption and analysis of the clpB, clpC and clpE genes in Lactobacillus lactis: ClpE, a new Clp family in Gram-Positive bacteria. J Bacteriol 181: 2075-2083.
  • Jofré A, Champomier-Vergés M, Anglade P, Baraige F, Martin B, Garriga M, Zagorec M, Aymerich T (2007) Protein synthesis in lactic acid and pathogenic bacteria during recovery from a high pressure treatment. Res Microbiol 158: 512-520. doi: 10.1016/j.resmic.2007.05.005.
  • Juvonen R, Virkajärvi V, Priha O, Laitila A (2011) Microbiological spoilage and safety risks in non-beer beverages. VTT Tiedotteita-Research Notes 2599. doi: 10.13140/RG.2.1.3166.8562
  • Korakli M, Ganzle MG, Knorr R, Frank M, Rossmann A, Vogel RF (2002) Metabolism of Lactobacillus sanfranciscensis under high pressure: investigations using stable carbon isotopes. Trends in High Pressure Bioscience and Biotechnology 19: 287-294. doi: 10.1016/S0921-0423(02)80114-9
  • Kruger E, Hecker M (1998) The first gene of the Bacillus subtilis clpC operon, ctsR, encodes a negative regulator of its own operon and other class III heat shock genes. J Bacteriol 180: 6681-6688.
  • Lawlor K, Schuman J, Simpson P, Taormina J (2009) In Compendium of the Microbiological Spoilage of Foods and Beverages, Food Microbiology and Safety, Sperber WH, Doyle MP eds, pp 245-283. Springer New York. doi: 10.1007/978-1-4419-0826-1.
  • Lorca G, Font de Valdez G (2009) Lactobacillus stress Responses In Lactobacillus Molecular Biology: From Genomic to Probiotics, Ljung A, Wadström T eds, pp 115-129. Caister Academy Press, Norfolk, UK. doi: 10.1002/elsc.200990012.
  • Mathias SP, Rosenthal A, Gaspar A, Aragao GM, Slongo-Marcusi A (2013) Prediction of acid lactic-bacteria growth in turkey ham processed by high hydrostatic pressure. Braz J Microbiol 44: 23-28. doi: 10.1590/S1517-83822013005000014.
  • Molenaar D, Bringel F, Schuren FH, de Vos WM, Siezen RJ, Kleerebezem M (2005) Exploring Lactobacillus plantarum genome diversity by using microarrays. J Bacteriol 187: 6119-6127. doi: 10.1128/JB.187.17.6119-6127.2005.
  • Mota MJ, Lopes RP, Delgadillo I, Saraiva JA (2013) Microorganisms under high pressure--adaptation, growth and biotechnological potential. Biotechnol Adv 31: 1426-1434. doi: 10.1016/j.biotechadv.2013.06.007.
  • Parente E, Ciocia F, Ricciardi A, Zotta T, Felis GE, Torriani S (2010) Diversity of stress tolerance in Lactobacillus plantarum, Lactobacillus pentosus and Lactobacillus paraplantarum: a multivariate screening study. Int J Food Microbiol 144: 270-279. doi: 10.1016/j.ijfoodmicro.2010.10.005.
  • Rendueles E, Omer MK, Alvseike O, Alonso-Calleja C, Capita R, Prieto M (2010) Microbiological food safety assessment of high hydrostatic pressure processing: A review. LWT - Food Science and Technology 44: 1251–1260. doi: 10.1016/j.lwt.2010.11.001
  • Ricciardi A, Parente E, Guidone A, Ianniello RG, Zotta T, Abu Sayem SM, Varcamonti M (2012) Genotypic diversity of stress response in Lactobacillus plantarum, Lactobacillus paraplantalum and Lactobacillus pentosus. Int J Food Microbiol 157: 278-285. doi: 10.1016/j.ijfoodmicro.2012.05.018.
  • Russo P, de la Luz Mohedano M, Capozzi V, de Palencia PF, López P, Spano G, Fiocco D (2012) Comparative proteomic analysis of Lactobacillus plantarum WCFS1 and ΔctsR mutant strains under physiological and heat stress conditions. Int J Mol Sci 13: 10680-10696.
  • Salminen S, von Wright A (2004) Lactic acid bacteria. Microbiology and functional aspects. pp 633. Marcel Dekker, New York, USA.
  • Sato T, Kato C, Horikoshi K (1995) The effect of high pressure on gene expression by the lac and tac promoters in Escherichia coli. J Marine Biotechnol 3: 89-92
  • Sauvageot N, Gouffi K, Laplace J, Auffray Y (2000) Glycerol metabolism in Lactobacillus collinoides: production of 3-hydroxypropionaldehyde, a precursor of acrolein. Int J Food Microbiol 55: 167-170. doi: 10.1016/S0168-1605(00)00191-4.
  • Scheyhing CH, Hörmann S, Ehrmann MA, Vogel RF (2004) Barotolerance is inducible by preincubation under hydrostatic pressure, cold-, osmotic-, and acid-stress conditions in Lactobacillus sanfranciscensis. DSM 2045 20451T. Lett Appl Microbiol 39: 284-289. doi: 10.1111/j.1472-765X.2004.01578.x.
  • Schumann W (2003) The Bacillus subtilis heat shock stimulon. Cell Stress Chaperones 8: 207-217.
  • Serrano LM, Molenaar D, Wels M, Teusink B, Bron PA, de Vos WM, Smid EJ (2007) Thioredoxin reductase is a key factor in the oxidative stress response of Lactobacillus plantarum WCFS1. Microbial Cell Factories 6: 29. doi: 10.1186/1475-2859-6-29.
  • Serrazanetti DI, Gottardi D, Montanari C, Gianotti A (2013) Dynamic stresses of lactic acid bacteria associated to fermentation processes. Lactic Acid Bacteria - R&D for Food, Health and Livestock Purposes 23: 539–570. doi: 10.5772/51049
  • Serrazanetti DI, Guerzoni ME, Corsetti A, Vogel RF (2009) Metabolic impact and potential exploitation of the stress reactions in lactobacilli. Food Microbiol 26: 700-711. doi: 10.1016/
  • Shah NP (2007) Functional cultures and health benefits. Int Dairy J 17: 1262-2127. doi: 10.1016/j.idairyj.2007.01.014
  • Siezen RJ, Tzeneva VA, Castioni A, Wels M, Phan HTK, Rademaker JLW, Starrenburg MJC, Kleerebezem M, Molenaar D, van Hylckama Vlieg JET (2010) Phenotypic and genomic diversity of Lactobacillus plantarum strains isolated from various environmental niches. Environ Microbiol 12: 758-773. doi: 10.1111/j.1462-2920.2009.02119.x.
  • Siragusa S, De Angelis M, Di Cagno R, Rizzello CG, Coda R, Gobbetti M (2007) Synthesis of γ-aminobutyric acid by lactic acid bacteria isolated from a variety of Italian cheeses. Appl Environ Microbiol 73: 7283-7290. doi: 10.1128/AEM.01064-07.
  • Smeds A, Varmanen P, Palva A (1998) Molecular characterization of a stress-inducible gene from Lactobacillus helveticus. J Bacteriol 180: 6148-6153.
  • Smits GJ, Brul S (2005) Stress tolerance in fungi - to kill a spoilage yeast. Curr Opin Biotechnol 16: 225–230. doi: 10.1016/j.copbio.2005.02.005.
  • Sokołowska B, Skąpska S, Fonberg-Broczek M, Niezgoda J, Rutkowska M, Chotkiewicz M, Dekowska A, Dobros N, Rzoska SJ (2012) Impact of high hydrostatic pressure on native microflora and colour of root vegetable juices. Post Nauki Technol Przem Rol-Spoż 67: 5-15 (in Polish)
  • Sokołowska B, Skąpska S, Fonberg-Broczek M, Niezgoda J, Rutkowska M, Dobros N, Rzoska JS (2014) The impact of high hydrostatic pressure (HHP) on native microflora and the colour of beetroot juice - a preliminary shelf-life study. In Industrial, Medical and Environmental Applications of Microorganisms: Current Status and Trends, Mendez-Vilas A, pp 380–384. Wageningen Academic Publisher. doi: 10.3920/978-90-8686-795-2.
  • Stortz G, Hengge-Aronis R eds (2000) Bacterial Stress Responses. pp 485. ASM Press, Washington, DC. doi: 10.1128/9781555816841.
  • Ulmer HM, Herberhold H, Fahsel S (2002) Effects of pressure-induced membrane phase transition on HorA inactivation in Lactobacillus plantarum. Appl Environ Microbiol 68: 1088-1095. doi: 10.1128/AEM.68.3.1088-1095.2002.
  • Van de Guchte M, Serror P, Chervaux Ch, Smokvina T, Ehrlich SD, Maguin E (2002) Stress responses in lactic acid bacteria. Antonie van Leeuwenhoek 82: 187-216. doi: 10.1023/A:1020631532202.
  • Varmanen P, Ingmer H, Vogensen FK (2000) ctsR of Lactococcus lactis encodes a negative regulator of clp gene expression. Microbiology 146: 1447-1455. doi: 10.1099/00221287-146-6-1447.
  • Vogel RF, Pavlovic M, Hörmann S, Ehrmann MA (2005) High pressure-sensitive gene expression in Lactobacillus sanfranciscensis. Braz J Med Biol Res 38: 1247-1252. doi: 10.1590/S0100-879X2005000800013.
  • Welch TJ, Farewell A, Neidhardt FC, Bartlett DH (1993) Stress response of Escherichia coli to elevated hydrostatic pressure. J Bacteriol 175: 7170-7177.
  • Wemekamp-Kamphuis HH, Karatzas AK, Wouters JA (2002) Enhanced levels of cold shock proteins in Listeria monocytogenes LO28 upon exposure to low temperature and high hydrostatic pressure. Appl Environ Microbiol 68: 456-463. doi: 10.1128/AEM.68.2.456-463.2002.
  • Wouters PC, Glaasker E, Smelt JP (1998) Effects of high pressure on inactivation kinetics and events related to proton efflux in Lactobacillus plantarum. Appl Environ Microbiol 64: 509-514.
  • Zuber U, Schumann W (1994) CIRCE, a novel heat shock element involved in regulation of heat shock operon dnaK of Bacillus subtilis. J Bacteriol 176: 1359-1363. doi: 10.1128/jb.176.5.1359-1363.1994.
Document Type
Publication order reference
YADDA identifier
JavaScript is turned off in your web browser. Turn it on to take full advantage of this site, then refresh the page.