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

Joanna Bucka-Kolendo; Barbara Sokołowska

doi:10.18388/abp.2017_1496

Joanna Bucka-Kolendo prof. Wacław Dąbrowski Institute of Agricultural and Food Biotechnology, Warsaw, Poland
Barbara Sokołowska prof. Wacław Dąbrowski Institute of Agricultural and Food Biotechnology, Warsaw, Poland

DOI: https://doi.org/10.18388/abp.2017_1496

Keywords: Lactic acid bacteria, LAB, stress factors, stress response, cross-protection

Abstract

Lactic Acid Bacteria (LAB) are the most widespread group of bacteria that are used in fermented foods. They are present in products like yogurts, sourdoughs, fermented vegetables, cheese, wine or meat, providing them positive sensory and nutritive features.

As harmless and desired microbes in one product, LAB can cause spoilage and a bad taste of the others, especially in juices and beverages. LAB are resistant to many of the stress factors which gives them the ability to survive in harsh environments. The most common stress factors they have to deal with are: heat, cold, acidity, NaCl and HHP-High Hydrostatic Pressure. Their ability to survive depends from their skills to cope with stress factors. Under stress conditions LAB activates mechanisms that allows 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 system they have, as resistance to one factor may help them to deal with the other stress factors. LAB have a high value for the food industry and that is why it is important to understand their mechanisms of stress response.

Author Biographies

Joanna Bucka-Kolendo, prof. Wacław Dąbrowski Institute of Agricultural and Food Biotechnology, Warsaw, Poland

Department of Fruit and Vegetable Products Technology

Barbara Sokołowska, prof. Wacław Dąbrowski Institute of Agricultural and Food Biotechnology, Warsaw, Poland

Department of Fruit and Vegetable Products Technology

References

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 Microbiology Letters, 230: 53–61. doi:10.1016/S0378-1097(03)00854-1.

Ananta E. and 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(3): 307-13. DOI: 10.1016/j.ijfoodmicro.2004.04.012.

Asano S, Suzuki K, Iijima K, Motoyama H, Kuriyama H and Kitagawa Y (2007) Effect of morphological changes in beer-spoilage lactic acid bacteria on membrane filtration in breweries. Journal of Bioscience and Bioengineering, 104: 334–338. doi: 10.1263/jbb.104.334.

Back W (2005) Colour Atlas and Handbook of Beverage Biology. W. Back (ed.). Verlag Hans Carl: Nürnberg, Germany, 317 pp.

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. Journal of Applied Microbiology, 100: 728–738. http://dx.doi.org/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.

Chastnet A, Fert J, Msadek T.( 2003) Comparative genomic 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.

Chastnet A, Msadek T. (2003) ClpP of Sreptococcus 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 and Drake M (2006) Stress response of Escherichia coli. Comprehensive reviews in Food Science and 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. 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. Applied and Environmental Microbiology, 70: 1336–1346. DOI: 10.1128/AEM.70.3.1336-1346.2004.

De Angelis M., Gobbetti, M. (2011) Stress responses of lactobacilli. In: Papadimitriou, K., Tsakalidou, E. (eds) Stress responses of lactic acid bacteria. Springer, New York, 219–249 pp. DOI: 10.1007/978-0-387-92771-8.

Derre´ I, G. Rapoport and 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.

Derre´, I, Rapoport, G and 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.

Derre´ I, Rapoport G, Devine K, Rose M and 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. International Journal of Food Microbiology, 143: 246–253. DOI: 10.1016/j.ijfoodmicro.2010.08.018.

Drews O, Weiss W, Reil G, Parlar H, Wait R. and 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 and Vogel RF. (2001) In vitro stability and expression of green fluorescent protein under high pressure conditions. Letters in Applied Microbiology, 32: 230–234. DOI: 10.1046/j.1472-765X.2001.00892.x

Fiocco D, Collins M, Muscariello L, Hols P, Kleerebezem M, Msadek T, and 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 from Tsakalidou, E. and K. Papadimitrious K. (eds) Stress responses of lactic acid bacteria. Springer Science & Business Media, 530, 13-15 pp. DOI: 10.1007/978-0-387-92771-8.

Garai-Ibabe G, Ibarburu I, Berregi I, Claisse O, Lonvaud-Funel A, Irastorza A and Dueñas MT. (2008) Glycerol metabolism and bitterness producing lactic acid bacteria in cidermaking. International Journal of Food Microbiology, 121: 253–261. DOI: 10.1016/j.ijfoodmicro..11.004.

Gökmen V, Acar J. (2004) Fumaric acid: The indicator of microbial spoilage of apple juice. Food Additives and Contaminant, 21(7): 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 and Hertel C. (2009) Genus I. Lactobacillus beijerinck 1901, 212AL. In: De Vos P, Garrity G, Jones D, Krieg NR, Ludwig W, Rainey FA, Schleifer KH and Whitman WB (eds.). Bergey’s Manual of Systematic Bacteriology, 2nd ed. New York, Springer. 465–513 pp. DOI: 10.1007/0-387-28022-7.

Hecker M, Schumann W and 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-Quintás N, Lopés P, Munduate A, Irastorza A and 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. International Journal of Food Microbiology, 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. Research in Microbiology, 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 and 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. http://dx.doi.org/10.1016/S0921-0423(02)80114-9.

Kruger E. and 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 and Taormina J. (2009) In: Sperber WH and Doyle MP. (eds.) Compendium of the Microbiological Spoilage of Foods and Beverages, Food Microbiology and Safety, Springer New York, 245–283 pp. DOI: 10.1007/978-1-4419-0826-1.

Lorca G and Font de Valdez G. (2009) Lactobacillus stress Responses In Ljung A, Wadström T.(eds.) Lactobacillus Molecular Biology: From Genomic to Probiotics. Caister Academy Press, Norfolk, UK, 115-129 pp. DOI: 10.1002/elsc.200990012.

Mathias SP, Rosenthal A, Gaspar A, Argao GMF, Slongo-Marcusi A. (2013) Prediction of acid lactic-bacteria growth in turkey ham processed by high hydrostatic pressure. Brazilian Journal of Microbiology, 44(1): 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(8): 1426-34. 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. http://dx.doi.org/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. International of Food Microbiology, 157: 278-285. DOI: 10.1016/j.ijfoodmicro.2012.05.018.

Russo P, Mohedano ML, Capozzi V, Fernández de Palencia P, López P, Spano G. (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, and von Wright A. (2004) Lactic acid bacteria. Microbiology and functional aspects. Marcel Dekker, New York, USA, 633 pp.

Sato T, Kato C and Horikoshi K. (1995) The effect of high pressure on gene expression by the lac and tac promoters in Escherichia coli. Journal of Marine Biotechnology, 3: 89–92.

Sauvageot N, Gouffi K, Laplace J and Auffray Y (2000) Glycerol metabolism in Lactobacillus collinoides: production of 3-hydroxypropionaldehyde, a precursor of acrolein. International Journal of Food Microbiology, 55:167–170. http://dx.doi.org/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. http://dx.doi.org/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/j.fm.2009.07.007.

Shah NP. (2007) Functional cultures and health benefits. International Dairy Journal 17: 1262–127. http://dx.doi.org/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. Environmental Microbiology, 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. Applied and Environmental Microbiology 73: 7283–7290. DOI: 10.1128/AEM.01064-07.

Smeds A, Varmanen P and Palva A. (1998) Molecular characterization of a stress-inducible gene from Lactobacillus helveticus. J Bacteriol.,180: 6148–6153.

Smits GJ and Brul S. (2005) Stress tolerance in fungi – to kill a spoilage yeast. Current Opinion in Biotechnology, 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) Wpływ wysokiego ciśnienia hydrostatycznego na naturalną mikroflorę i barwę soków z warzyw korzeniowych, Post. Nauki Technol. Przem. Rol.-Spoż., 67(4): 5-15.

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, Wageningen Academic Publisher., 380-384 pp.

Stortz G and Hengge-Aronis R (Eds.) (2000) Bacterial Stress Responses. ASM Press, Washington, DC, 485 pp. DOI: 10.1128/9781555816841.

Ulmer HM, Herberhold H, Fahsel S. (2002) Effects of pressure induced membrane phase transition on HorA inactivation in Lactobacillus plantarum. Applied and Environmental Microbiology, 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 expression in Lactobacillus sanfranciscensis. Brazilian Journal of Medical and Biological Research, 38: 1247-1252. DOI: /S0100-879X2005000800013.

Welch TJ, Farewell A, Neidhardt FC and Bartlett DH. (1993) Stress response of Escherichia coli to elevated hydrostatic pressure. Journal of Bacteriology, 175: 7170–7177.

Wemekamp-Kamphuis HH, Karatzas AK and Wouters JA. (2002) Enhanced levels of cold shock proteins in Listeria monocytogenes LO28 upon exposure to low temperature and high hydrostatic pressure. Applied and Environmental Microbiology, 68: 456–463. DOI: 10.1128/AEM.68.2.456-463.2002.

Wouters PC, Glaasker E and Smelt JPPM. (1998) Effects of high pressure on inactivation kinetics and events related to proton efflux in Lactobacillus plantarum. Applied and Environmental Microbiology, 64: 509–514.

Zuber U and Schumann W. (1994) CIRCE, a novel heat shock element involved in regulation of heat shock operon dnaK of Bacillus subtilis. J Bacteriol., 176(5): 1359-63. DOI: 10.1128/jb.176.5.1359-1363.1994.