Abstract
Production of lactic acid bacteria starters for manufacturing food, probiotic, and chemical products requires the application of successive steps: fermentation, concentration, stabilization, and storage. Despite process optimization, losses of bacterial viability and functional activities are observed after stabilization and storage steps due to cell exposure to environmental stresses (thermal, osmotic, mechanical, and oxidative). Bacterial membrane is the primary target for injury and its damage is highly dependent on its physical properties and lipid organization. Membrane fluidity is a key property for maintaining cell functionality, and depends on lipid composition and cell environment. Extensive evidence has been reported on changes in membrane fatty acyl chains when modifying fermentation conditions. However, a deep characterization of membrane physical properties and their evolution following production processes is scarcely reported. Therefore, the aims of this mini-review are (i) to define the membrane fluidity and the methods used to assess it and (ii) to summarize the effect of environmental conditions on membrane fluidity and the resulting impact on the resistance of lactic acid bacteria to the stabilization processes. This will make it possible to highlight existing gaps of knowledge and opens up novel approaches for future investigations.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Andersen AB, Fog-Petersen MS, Larsen H, Skibsted LH (1999) Storage stability of freeze-dried starter cultures (Streptococcus thermophilus) as related to physical state of freezing matrix. Lebensm Wiss Technol 32:540–547
Barák I, Muchová K (2013) The role of lipid domains in bacterial cell processes. Int J Mol Sci 14:4050–4065. https://doi.org/10.3390/ijms14024050
Barák I, Muchová K, Wilkinson AJ, O’Toole PJ, Pavlendová N (2008) Lipid spirals in Bacillus subtilis and their role in cell division. Mol Microbiol 68:1315–1327. https://doi.org/10.1111/j.1365-2958.2008.06236.x
Béal C, Fonseca F (2015) Freezing of probiotic bacteria. In: Foerst P, Santivarangkna C (eds) Advances in probiotic technology. CRC Press, Boca Raton, pp 179–212
Béal C, Fonseca F, Corrieu G (2001) Resistance to freezing and frozen storage of Streptococcus thermophilus is related to membrane fatty acid composition. J Dairy Sci 84:2347–2356. https://doi.org/10.3168/jds.S0022-0302(01)74683-8
Beney L, Gervais P (2001) Influence of the fluidity of the membrane on the response of microorganisms to environmental stresses. Appl Microbiol Biotechnol 57:34–42
Bernal P, Segura A, Ramos J-L (2007) Compensatory role of the cis - trans -isomerase and cardiolipin synthase in the membrane fluidity of Pseudomonas putida DOT-T1E: Cis - trans -isomerase and cardiolipin synthase. Environ Microbiol 9:1658–1664. https://doi.org/10.1111/j.1462-2920.2007.01283.x
Bouix M, Ghorbal S (2017) Assessment of bacterial membrane fluidity by flow cytometry. J Microbiol Methods 143:50–57. https://doi.org/10.1016/j.mimet.2017.10.005
Brennan M, Wanismail B, Johnson MC, Ray B (1986) Cellular damage in dried Lactobacillus acidophilus. J Food Prot 49(1):47–53. https://doi.org/10.4315/0362-028X-49.1.47
Broadbent JR, Larsen RL, Deibel V, Steele JL (2010) Physiological and transcriptional response of Lactobacillus casei ATCC 334 to acid stress. J Bacteriol 192:2445–2458. https://doi.org/10.1128/JB.01618-09
Carpenter JF, Crowe JH (1988) The mechanism of cryoprotection of proteins by solutes. Cryobiology 25:244–255
Castro HP, Teixeira PM, Kirby R (1995) Storage of lyophilized cultures of Lactobacillus bulgaricus under different relative humidities and atmospheres. Appl Microbiol Biotechnol 44:172–176
Castro HP, Teixeira PM, Kirby R (1996) Changes in the cell membrane of Lactobacillus bulgaricus during storage following freeze-drying. Biotechnol Lett 18:99–104
Chu-Ky S, Tourdot-Marechal R, Marechal P-A, Guzzo J (2005) Combined cold, acid, ethanol shocks in Oenococcus oeni: effects on membrane fluidity and cell viability. Biochim Biophys Acta BBA - Biomembr 1717:118–124. https://doi.org/10.1016/j.bbamem.2005.09.015
Coulibaly I, Amenan AY, Lognay G, Fauconnier ML, Thonart P (2009) Survival of freeze-dried Leuconostoc mesenteroides and Lactobacillus plantarum related to their cellular fatty acids composition during storage. Appl Biochem Biotechnol 157:70–84. https://doi.org/10.1007/s12010-008-8240-1
Crowe JH (2015) Anhydrobiosis: an unsolved problem with applications in human welfare. In: Disalvo EA (ed) Membrane Hydration. Springer International Publishing, Cham, pp 263–280
Crowe JH, Crowe LM, Carpenter JF, Rudolph AS, Wistrom CA, Spargo BJ, Anchordoguy TJ (1988) Interactions of sugars with membranes. Biochim Biophys Acta 947:367–384
Crowe JH, Crowe LM, Hoekstra FA, Wistrom CA (1989) Effects of water on the stability of phospholipid bilayers: the problem of imbibition damage in dry organisms. In: CSSA Special Publication n°14. Crop science Society of America, USA
Da Silveira MG, Golovina EA, Hoekstra FA, Rombouts FM, Abee T (2003) Membrane fluidity adjustments in ethanol-stressed Oenococcus oeni cells. Appl Environ Microbiol 69:5826–5832. https://doi.org/10.1128/AEM.69.10.5826-5832.2003
Deleu M, Crowet J-M, Nasir MN, Lins L (2014) Complementary biophysical tools to investigate lipid specificity in the interaction between bioactive molecules and the plasma membrane: a review. Biochim Biophys Acta BBA - Biomembr 1838:3171–3190. https://doi.org/10.1016/j.bbamem.2014.08.023
Denich TJ, Beaudette LA, Lee H, Trevors JT (2003) Effect of selected environmental and physico-chemical factors on bacterial cytoplasmic membranes. J Microbiol Methods 52:149–182. https://doi.org/10.1016/S0167-7012(02)00155-0
Donovan C, Bramkamp M (2009) Characterization and subcellular localization of a bacterial flotillin homologue. Microbiology 155:1786–1799. https://doi.org/10.1099/mic.0.025312-0
Drucker DB, Megson G, Harty DW, Riba I, Gaskell SJ (1995) Phospholipids of Lactobacillus spp. J Bacteriol 177:6304–6308. https://doi.org/10.1128/jb.177.21.6304-6308.1995
Dumont F, Marechal P-A, Gervais P (2004) Cell size and water permeability as determining factors for cell viability after freezing at different cooling rates. Appl Environ Microbiol 70:268–272. https://doi.org/10.1128/AEM.70.1.268-272.2004
El Khoury M, Swain J, Sautrey G, Zimmermann L, Van Der Smissen P, Décout J-L, Mingeot-Leclercq M-P (2017) Targeting bacterial cardiolipin enriched microdomains: an antimicrobial strategy used by amphiphilic aminoglycoside antibiotics. Sci Rep 7:10697. https://doi.org/10.1038/s41598-017-10543-3
Epand RM (1998) Lipid polymorphism and protein–lipid interactions. Biochim Biophys Acta BBA - Rev Biomembr 1376:353–368. https://doi.org/10.1016/S0304-4157(98)00015-X
Fernández Murga ML, Bernik D, Font de Valdez G, Disalvo AE (1999) Permeability and stability properties of membranes formed by lipids extracted from Lactobacillus acidophilus grown at different temperatures. Arch Biochem Biophys 364:115–121. https://doi.org/10.1006/abbi.1998.1093
Fernández-Murga ML, Cabrera GM, de Valdez GF, Disalvo A, Seldes AM (2000) Influence of growth temperature on cryotolerance and lipid composition of Lactobacillus acidophilus. J Appl Microbiol 88:342–348. https://doi.org/10.1046/j.1365-2672.2000.00967.x
Fonseca F, Marin M, Morris GJ (2006) Stabilization of frozen Lactobacillus delbrueckii subsp. bulgaricus in glycerol suspensions: freezing kinetics and storage temperature effects. Appl Environ Microbiol 72:6474–6482. https://doi.org/10.1128/aem.00998-06
Fonseca F, Cenard S, Passot S (2015) Freeze-drying of lactic acid bacteria. In: Wolkers WF, Oldenhof H (eds) Cryopreservation and freeze-drying protocols. Springer New York, New York, NY, pp 477–488
Fonseca F, Meneghel J, Cenard S, Passot S, Morris GJ (2016) Determination of intracellular vitrification temperatures for unicellular micro organisms under conditions relevant for cryopreservation. PLoS One 11:e0152939. https://doi.org/10.1371/journal.pone.0152939
Fozo E, Kajfasz J, Quivey RG Jr (2004) Low pH-induced membrane fatty acid alterations in oral bacteria. FEMS Microbiol Lett 238:291–295. https://doi.org/10.1016/j.femsle.2004.07.047
Garbay S, Lonvaud-Funel A (1996) Response of Leuconostoc œnos to environmental changes. J Appl Bacteriol 81:619–625. https://doi.org/10.1111/j.1365-2672.1996.tb03556.x
García AH (2011) Anhydrobiosis in bacteria: from physiology to applications. J Biosci 36:939–950. https://doi.org/10.1007/s12038-011-9107-0
Gautier J, Passot S, Pénicaud C, Guillemin H, Cenard S, Lieben P, Fonseca F (2013) A low membrane lipid phase transition temperature is associated with a high cryotolerance of Lactobacillus delbrueckii subsp. bulgaricus CFL1. J Dairy Sci 96:5591–5602. https://doi.org/10.3168/jds.2013-6802
Gilarová R, Voldřich M, Demnerová K, Čeřovský M, Dobiáš J (1994) Cellular fatty acids analysis in the identification of lactic acid bacteria. Int J Food Microbiol 24:315–319. https://doi.org/10.1016/0168-1605(94)90129-5
Gilliland SE, Speck ML (1974) Relationship of cellular components to the stability of concentrated lactic streptococcus cultures at -17°C. Appl Microbiol 27:793–796
Goldberg I, Eschar L (1977) Stability of lactic acid bacteria to freezing as related to their fatty acid composition. Appl Environnmental Microbiol 33:489–496
Gómez-Zavaglia A, Disalvo EA, De Antoni GL (2000) Fatty acid composition and freeze-thaw resistance in lactobacilli. J Dairy Res 67:241–247
Guerzoni ME, Lanciotti R, Cocconcelli PS (2001) Alteration in cellular fatty acid composition as a response to salt, acid, oxidative and thermal stresses in Lactobacillus helveticus. Microbiology 147:2255–2264. https://doi.org/10.1099/00221287-147-8-2255
Guillot A, Obis D, Mistou M-Y (2000) Fatty acid membrane composition and activation of glycine-betaine transport in Lactococcus lactis subjected to osmotic stress. Int J Food Microbiol 55:47–51. https://doi.org/10.1016/S0168-1605(00)00193-8
Hachmann A-B, Angert ER, Helmann JD (2009) Genetic analysis of factors affecting susceptibility of Bacillus subtilis to daptomycin. Antimicrob Agents Chemother 53:1598–1609. https://doi.org/10.1128/AAC.01329-08
Harris FM, Best KB, Bell JD (2002) Use of laurdan fluorescence intensity and polarization to distinguish between changes in membrane fluidity and phospholipid order. Biochim Biophys Acta BBA - Biomembr 1565:123–128. https://doi.org/10.1016/S0005-2736(02)00514-X
Hazel JR (1995) Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation? Annu Rev Physiol 57:19–42. https://doi.org/10.1146/annurev.ph.57.030195.000315
Hazel JR, Williams EE (1990) The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res 29:167–227
Heipieper HJ, Weber FJ, Sikkema J, Keweloh H, de Bont JAM (1994) Mechanisms of resistance of whole cells to toxic organic solvents. Trends Biotechnol 12:409–415. https://doi.org/10.1016/0167-7799(94)90029-9
Hutter E, Assiongbon KA, Fendler JH, Roy D (2003) Fourier transform infrared spectroscopy using polarization modulation and polarization selective techniques for internal and external reflection geometries: investigation of self-assembled octadecylmercaptan on a thin gold film. J Phys Chem B 107:7812–7819. https://doi.org/10.1021/jp034910p
In’t Veld G, Driessen AJM, Konings WN (1992) Effect of the unsaturation of phospholipid acyl chains on leucine transport of Lactococcus lactis and membrane permeability. Biochim Biophys Acta 1108:31–39
Johnsson T, Nikkilä P, Toivonen L, Rosenqvist H, Laakso S (1995) Cellular fatty acid profiles of Lactobacillus and Lactococcus strains in relation to the oleic acid content of the cultivation medium. Appl Environ Microbiol 61:4497–4499
Kaneda T (1991) Iso-and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microbiol Rev 55:288–302
Kawai F, Shoda M, Harashima R, Sadaie Y, Hara H, Matsumoto K (2004) Cardiolipin domains in Bacillus subtilis marburg membranes. J Bacteriol 186:1475–1483. https://doi.org/10.1128/JB.186.5.1475-1483.2004
Kent B, Hauß T, Demé B, Cristiglio V, Darwish T, Hunt T, Bryant G, Garvey CJ (2015) Direct comparison of disaccharide interaction with lipid membranes at reduced hydrations. Langmuir 31:9134–9141. https://doi.org/10.1021/acs.langmuir.5b02127
Koynova R, Tenchov B (2013) Recent patents on nonlamellar liquid crystalline lipid phases in drug delivery. Recent Pat Drug Deliv Formul 7:165–173. https://doi.org/10.2174/18722113113079990011
Kurtmann L, Carlsen CU, Skibsted LH, Risbo J (2009) Water activity-temperature state diagrams of freeze-dried Lactobacillus acidophilus (La-5): influence of physical state on bacterial survival during storage. Biotechnol Prog 25:265–270
Lee AG (2004) How lipids affect the activities of integral membrane proteins. Biochim Biophys Acta BBA - Biomembr 1666:62–87. https://doi.org/10.1016/j.bbamem.2004.05.012
Leslie SB, Israeli E, Lighthart B, Crowe JH, Crowe LM (1995) Trehalose and sucrose protect both membranes and proteins in intact bacteria during drying. Appl Environ Microbiol 61:3592–3597
Letellier L, Moudden H, Shechter E (1977) Lipid and protein segregation in Escherichia coli membrane: morphological and structural study of different cytoplasmic membrane fractions. Proc Natl Acad Sci 74:452–456. https://doi.org/10.1073/pnas.74.2.452
Lewis RNAH, McElhaney RN (2013) Membrane lipid phase transitions and phase organization studied by Fourier transform infrared spectroscopy. Biochim Biophys Acta BBA - Biomembr 1828:2347–2358. https://doi.org/10.1016/j.bbamem.2012.10.018
Li C, Zhao J-L, Wang Y-T, Han X, Liu N (2009a) Synthesis of cyclopropane fatty acid and its effect on freeze-drying survival of Lactobacillus bulgaricus L2 at different growth conditions. World J Microbiol Biotechnol 25:1659–1665. https://doi.org/10.1007/s11274-009-0060-0
Li H, Zhao W, Wang H, Li Z, Wang A (2009b) Influence of culture pH on freeze-drying viability of Oenococcus oeni and its relationship with fatty acid composition. Food Bioprod Process 87:56–61. https://doi.org/10.1016/j.fbp.2008.06.001
Lin T-Y, Weibel DB (2016) Organization and function of anionic phospholipids in bacteria. Appl Microbiol Biotechnol 100:4255–4267. https://doi.org/10.1007/s00253-016-7468-x
Linders LJM, Wolkers WF, Hoekstra FA, Van ‘t Riet K (1997) Effect of added carbohydrates on membrane phase behavior and survival of dried Lactobacillus plantarum. Cryobiology 35:31–40
Loffhagen N, Hartig C, Babel W (2001) Suitability of the trans/cis ratio of unsaturated fatty acids in Pseudomonas putida NCTC 10936 as an indicator of the acute toxicity of chemicals. Ecotoxicol Environ Saf 50:65–71
López CS (2006) Role of anionic phospholipids in the adaptation of Bacillus subtilis to high salinity. Microbiology 152:605–616. https://doi.org/10.1099/mic.0.28345-0
López D, Kolter R (2010) Functional microdomains in bacterial membranes. Genes Dev 24:1893–1902. https://doi.org/10.1101/gad.1945010
Los DA, Murata N (2004) Membrane fluidity and its roles in the perception of environmental signals. Biochim Biophys Acta BBA - Biomembr 1666:142–157. https://doi.org/10.1016/j.bbamem.2004.08.002
Louesdon S, Charlot-Rougé S, Tourdot-Maréchal R, Bouix M, Béal C (2015) Membrane fatty acid composition and fluidity are involved in the resistance to freezing of Lactobacillus buchneri R1102 and Bifidobacterium longum R0175. Microb Biotechnol 8:311–318. https://doi.org/10.1111/1751-7915.12132
Luzardo M d C, Amalfa F, Nuñez AM, Díaz S, Biondi de López AC, Disalvo EA (2000) Effect of trehalose and sucrose on the hydration and dipole potential of lipid bilayers. Biophys J 78:2452–2458. https://doi.org/10.1016/S0006-3495(00)76789-0
Machado MC, López CS, Heras H, Rivas EA (2004) Osmotic response in Lactobacillus casei ATCC 393: biochemical and biophysical characteristics of membrane. Arch Biochem Biophys 422:61–70. https://doi.org/10.1016/j.abb.2003.11.001
Mansilla MC, Cybulski LE, Albanesi D, de Mendoza D (2004) Control of membrane lipid fluidity by molecular thermosensors. J Bacteriol 186:6681–6688. https://doi.org/10.1128/JB.186.20.6681-6688.2004
Mendelsohn R, Moore DJ (1998) Vibrational spectroscopic studies of lipid domains in biomembranes and model systems. Chem Phys Lipids 96:141–157
Meneghel J, Passot S, Cenard S, Réfrégiers M, Jamme F, Fonseca F (2017a) Subcellular membrane fluidity of Lactobacillus delbrueckii subsp. bulgaricus under cold and osmotic stress. Appl Microbiol Biotechnol 101:6907–6917. https://doi.org/10.1007/s00253-017-8444-9
Meneghel J, Passot S, Dupont S, Fonseca F (2017b) Biophysical characterization of the Lactobacillus delbrueckii subsp. bulgaricus membrane during cold and osmotic stress and its relevance for cryopreservation. Appl Microbiol Biotechnol 101:1427–1441. https://doi.org/10.1007/s00253-016-7935-4
Milhaud J (2004) New insights into water–phospholipid model membrane interactions. Biochim Biophys Acta BBA - Biomembr 1663:19–51. https://doi.org/10.1016/j.bbamem.2004.02.003
Molina-Höppner A, Doster W, Vogel RF, Ganzle MG (2004) Protective effect of sucrose and sodium chloride for Lactococcus lactis during sublethal and lethal high-pressure treatments. Appl Environ Microbiol 70:2013–2020. https://doi.org/10.1128/AEM.70.4.2013-2020.2004
Muchová K, Jamroškovič J, Barák I (2010) Lipid domains in Bacillus subtilis anucleate cells. Res Microbiol 161:783–790. https://doi.org/10.1016/j.resmic.2010.07.006
Mykytczuk NCS, Trevors JT, Leduc LG, Ferroni GD (2007) Fluorescence polarization in studies of bacterial cytoplasmic membrane fluidity under environmental stress. Prog Biophys Mol Biol 95:60–82. https://doi.org/10.1016/j.pbiomolbio.2007.05.001
Nikkilä P, Johnsson T, Rosenqvist H, Toivonen L (1996) Effect of pH on growth and fatty acid composition of Lactobacillus fermentum. Appl Biochem Biotechnol 59:245–257
Oldenhof H, Wolkers WF, Fonseca F, Passot S, Marin M (2005) Effect of sucrose and maltodextrin on the physical properties and survival of air-dried Lactobacillus bulgaricus: an in situ Fourier transform infrared spectroscopy study. Biotechnol Prog 21:885–892
Papadimitriou K, Alegría Á, Bron PA, de Angelis M, Gobbetti M, Kleerebezem M, Lemos JA, Linares DM, Ross P, Stanton C, Turroni F, van Sinderen D, Varmanen P, Ventura M, Zúñiga M, Tsakalidou E, Kok J (2016) Stress physiology of lactic acid bacteria. Microbiol Mol Biol Rev 80:837–890. https://doi.org/10.1128/MMBR.00076-15
Passot S, Jamme F, Réfrégiers M, Gautier J, Cenard S, Fonseca F (2014) Synchrotron UV fluorescence microscopy for determining membrane fluidity modification of single bacteria with temperatures. Biomed Spectrosc Imaging 203–210. https://doi.org/10.3233/BSI-140062
Perly B, Smith ICP, Jarrell HC (1985) Effects of the replacement of a double bond by a cyclopropane ring in phosphatidylethanolamines: a 2H NMR study of phase transitions and molecular organization. Biochemistry 24:1055–1062
Poger D, Mark AE (2015) A ring to rule them all: the effect of cyclopropane fatty acids on the fluidity of lipid bilayers. J Phys Chem B 119:5487–5495. https://doi.org/10.1021/acs.jpcb.5b00958
Potts M (1994) Desiccation tolerance of prokaryotes. Microbiol Rev 58:51
Romantsov T, Guan Z, Wood JM (2009) Cardiolipin and the osmotic stress responses of bacteria. Biochim Biophys Acta BBA - Biomembr 1788:2092–2100. https://doi.org/10.1016/j.bbamem.2009.06.010
Russell NJ, Evans RI, ter Steeg PF, Hellemons J, Verheul A, Abee T (1995) Membranes as a target for stress adaptation. Int J Food Microbiol 28:255–261
Santivarangkna C, Kulozik U, Foerst P (2008) Inactivation mechanisms of lactic acid starter cultures preserved by drying processes. J Appl Microbiol 105:1–13. https://doi.org/10.1111/j.1365-2672.2008.03744.x
Schechter E (2004) Biochimie et biophysique des membranes – Aspects structuraux et fonctionnels. Paris
Schneiter R, Toulmay A (2007) The role of lipids in the biogenesis of integral membrane proteins. Appl Microbiol Biotechnol 73:1224–1232
Schoug Å, Fischer J, Heipieper HJ, Schnürer J, Håkansson S (2008) Impact of fermentation pH and temperature on freeze-drying survival and membrane lipid composition of Lactobacillus coryniformis Si3. J Ind Microbiol Biotechnol 35:175–181. https://doi.org/10.1007/s10295-007-0281-x
Schwab C, Vogel R, Gänzle MG (2007) Influence of oligosaccharides on the viability and membrane properties of Lactobacillus reuteri TMW1.106 during freeze-drying. Cryobiology 55:108–114. https://doi.org/10.1016/j.cryobiol.2007.06.004
Seydlová G, Fišer R, Čabala R, Kozlík P, Svobodová J, Pátek M (2013) Surfactin production enhances the level of cardiolipin in the cytoplasmic membrane of Bacillus subtilis. Biochim Biophys Acta BBA - Biomembr 1828:2370–2378. https://doi.org/10.1016/j.bbamem.2013.06.032
Silvestro L, Axelsen PH (1998) Infrared spectroscopy of supported lipid monolayer, bilayer, and multibilayer membranes. Chem Phys Lipids 96:69–80
Smittle RB, Gilliland SE, Speck ML, Walter WMJ (1974) Relationship of cellular fatty acid composition to survival of Lactobacillus bulgaricus in liquid nitrogen. Appl Microbiol 27:738–743
Souzu H (1986) Fluorescence polarization studies on Escherichia coli membrane stability and its relation to the resistance of the cell to freeze-thawing. I. Membrane stability in cells of differing growth phase. Biochim Biophys Acta BBA - Biomembr 861:353–360. https://doi.org/10.1016/0005-2736(86)90438-4
Sperotto MM, Ipsen JH, Mouritsen OG (1989) Theory of protein-induced lateral phase separation in lilpid membranes. Cell Biophys 14:79. https://doi.org/10.1007/BF02797393
Streit F, Delettre J, Corrieu G, Béal C (2008) Acid adaptation of Lactobacillus delbrueckii subsp. bulgaricus induces physiological responses at membrane and cytosolic levels that improves cryotolerance. J Appl Microbiol 105:1071–1080. https://doi.org/10.1111/j.1365-2672.2008.03848.x
Suutari M, Laakso S (1992) Temperature adaptation in Lactobacillus fermentum: interconversions of oleic, vaccenic and dihydrosterulic acids. J Gen Microbiol 138:445–450
Teixeira P, Castro H, Kirby R (1996) Evidence of membrane lipid oxidation of spray-dried Lactobacillus bulgaricus during storage. Lett Appl Microbiol 22:34–38. https://doi.org/10.1111/j.1472-765X.1996.tb01103.x
Teixeira H, Goncalves MG, Rozes N, Ramos A, San Romao MV (2002) Lactobacillic acid accumulation in the plasma membrane of Oenococcus oeni: a response to ethanol stress? Microb Ecol 43:146–153. https://doi.org/10.1007/s00248-001-0036-6
To TMH, Grandvalet C, Tourdot-Maréchal R (2011) Cyyclopropanation of membrane unsaturated fatty acids is not essential to the acid stress response of Lactococcus lactis subsp. cremoris. Appl Environ Microbiol 77:3327–3334. https://doi.org/10.1128/AEM.02518-10
Torok Z, Horvath I, Goloubinoff P, Kovacs E, Glatz A, Balogh G, Vigh L (1997) Evidence for a lipochaperonin: association of active proteinfolding GroESL oligomers with lipids can stabilize membranes under heat shock conditions. Proc Natl Acad Sci 94:2192–2197. https://doi.org/10.1073/pnas.94.6.2192
Tourdot-Maréchal R, Gaboriau D, Beney L, Diviès C (2000) Mmembrane fluidity of stressed cells of Oenococcus oeni. Int J Food Microbiol 55:269–273. https://doi.org/10.1016/S0168-1605(00)00202-6
Trevors JT (2003) Fluorescent probes for bacterial cytoplasmic membrane research. J Biochem Biophys Methods 57:87–103
Tymczyszyn EE, Gómez-Zavaglia A, Disalvo EA (2005) Influence of the growth at high osmolality on the lipid composition, water permeability and osmotic response of Lactobacillus bulgaricus. Arch Biochem Biophys 443:66–73. https://doi.org/10.1016/j.abb.2005.09.004
Tymczyszyn EE, Del Rosario DM, Gómez-Zavaglia A, Disalvo EA (2007) Volume recovery, surface properties and membrane integrity of Lactobacillus delbrueckii subsp. bulgaricus dehydrated in the presence of trehalose or sucrose: volume recovery, surface properties and membrane integrity of dehydrated L. bulgaricus. J Appl Microbiol 103:2410–2419. https://doi.org/10.1111/j.1365-2672.2007.03482.x
Veerkamp JH (1971) Fatty acid composition of Bifidobacterium and Lactobacillus strains. J Bacteriol 108:861–867
Velly H, Bouix M, Passot S, Pénicaud C, Beinsteiner H, Ghorbal S, Lieben P, Fonseca F (2015) Cyclopropanation of unsaturated fatty acids and membrane rigidification improve the freeze-drying resistance of Lactococcus lactis subsp. lactis TOMSC161. Appl Microbiol Biotechnol 99:907–918. https://doi.org/10.1007/s00253-014-6152-2
Wang Y, Delettre J, Guillot A, Corrieu G, Béal C (2005) Influence of cooling temperature and duration on cold adaptation of Lactobacillus acidophilus RD758. Cryobiology 50:294–307. https://doi.org/10.1016/j.cryobiol.2005.03.001
Wang Y, Delettre J, Corrieu G, Béal C (2011) Starvation induces physiological changes that act on the cryotolerance of Lactobacillus acidophilus RD758. Biotechnol Prog 27:342–350. https://doi.org/10.1002/btpr.566
Wu C, Zhang J, Wang M, Du G, Chen J (2012) Lactobacillus casei combats acid stress by maintaining cell membrane functionality. J Ind Microbiol Biotechnol 39:1031–1039. https://doi.org/10.1007/s10295-012-1104-2
Zhang Y-M, Rock CO (2008) Membrane lipid homeostasis in bacteria. Nat Rev Microbiol 6:222–233. https://doi.org/10.1038/nrmicro1839
Funding
This work has received funding from the European Union’s Horizon 2020 Marie Skłodowska-Curie research and innovation program under grant agreement no. 777657.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Fonseca, F., Pénicaud, C., Tymczyszyn, E.E. et al. Factors influencing the membrane fluidity and the impact on production of lactic acid bacteria starters. Appl Microbiol Biotechnol 103, 6867–6883 (2019). https://doi.org/10.1007/s00253-019-10002-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-019-10002-1