Review

Exopolysaccharide production by lactic acid bacteria: the manipulation of environmental stresses for industrial applications

  • Received: 02 September 2020 Accepted: 12 November 2020 Published: 17 November 2020
  • Exopolysaccharides (EPSs) are biological polymers secreted by microorganisms including Lactic acid bacteria (LAB) to cope with harsh environmental conditions. EPSs are one of the main components involved in the formation of extracellular biofilm matrix to protect microorganisms from adverse factors such as temperature, pH, antibiotics, host immune defenses, etc.. In this review, we discuss EPS biosynthesis; the role of EPSs in LAB stress tolerance; the impact of environmental stresses on EPS production and on the expression of genes involved in EPS synthesis. The evaluation results indicated that environmental stresses can alter EPS biosynthesis in LAB. For further studies, environmental stresses may be used to generate a new EPS type with high biological activity for industrial applications.

    Citation: Phu-Tho Nguyen, Tho-Thi Nguyen, Duc-Cuong Bui, Phuoc-Toan Hong, Quoc-Khanh Hoang, Huu-Thanh Nguyen. Exopolysaccharide production by lactic acid bacteria: the manipulation of environmental stresses for industrial applications[J]. AIMS Microbiology, 2020, 6(4): 451-469. doi: 10.3934/microbiol.2020027

    Related Papers:

  • Exopolysaccharides (EPSs) are biological polymers secreted by microorganisms including Lactic acid bacteria (LAB) to cope with harsh environmental conditions. EPSs are one of the main components involved in the formation of extracellular biofilm matrix to protect microorganisms from adverse factors such as temperature, pH, antibiotics, host immune defenses, etc.. In this review, we discuss EPS biosynthesis; the role of EPSs in LAB stress tolerance; the impact of environmental stresses on EPS production and on the expression of genes involved in EPS synthesis. The evaluation results indicated that environmental stresses can alter EPS biosynthesis in LAB. For further studies, environmental stresses may be used to generate a new EPS type with high biological activity for industrial applications.


    加载中

    Acknowledgments



    Phu-Tho Nguyen is a graduate student researcher of Graduate University of Sciences and Technology, Vietnam Academy of Science and Technology, Vietnam. The authors would like to acknowledge the Science and Technology Program for the Southwestern Sustainable Development, Vietnam National University Ho Chi Minh City for the financial support. This publication's contents and interpretations are the sole responsibility of the authors.

    Conflicts of interest



    The authors declare no conflict of interest.

    [1] Paul P, Ramraj SK, Neelakandan Y, et al. (2011) Production and purification of a novel exopolysaccharide from lactic acid bacterium Streptococcus phocae PI80 and its functional characteristics activity in vitro. Bioresour Technol 102: 4827-4833. doi: 10.1016/j.biortech.2010.12.118
    [2] Singh P, Saini P (2017) Food and health potentials of exopolysaccharides derived from LactobacilliMicrobiol Res J Int 22: 1-14. doi: 10.9734/MRJI/2017/36935
    [3] Garai-Ibabe G, Dueñas M, Irastorza A, et al. (2010) Naturally occurring 2-substituted (1,3)-β-D-glucan producing Lactobacillus suebicus and Pediococcus parvulus strains with potential utility in the production of functional foods. Bioresour Technol 101: 9254-9263. doi: 10.1016/j.biortech.2010.07.050
    [4] Liu C, Lu J, Lu L, et al. (2010) Isolation, structural characterization and immunological activity of an exopolysaccharide produced by Bacillus licheniformis 8-37-0-1. Bioresour Technol 101: 5528-5533. doi: 10.1016/j.biortech.2010.01.151
    [5] Pan D, Mei X (2010) Antioxidant activity of an exopolysaccharide purified from Lactococcus lactis subsp. lactis 12. Carbohydr Polym 80: 908-914. doi: 10.1016/j.carbpol.2010.01.005
    [6] Nakajima H, Suzuki Y, Hirota T (2006) Cholesterol lowering activity of ropy fermented milk. J Food Sci 57: 1327-1329. doi: 10.1111/j.1365-2621.1992.tb06848.x
    [7] Patel A, Prajapati J (2013) Food and health applications of exopolysaccharides produced by Lactic acid Bacteria. Adv Dairy Res 1: 1-7.
    [8] Surayot U, Wang J, Seesuriyachan P, et al. (2014) Exopolysaccharides from lactic acid bacteria: Structural analysis, molecular weight effect on immunomodulation. Int J Biol Macromol 68: 223-240. doi: 10.1016/j.ijbiomac.2014.05.005
    [9] Polak-Berecka M, Waśko A, Paduch R, et al. (2014) The effect of cell surface components on adhesion ability of Lactobacillus rhamnosusAntonie van Leeuwenhoek 106: 751-762. doi: 10.1007/s10482-014-0245-x
    [10] Badel-Berchoux S, Bernardi T, Michaud P (2011) New perspective for Lactobacilli exopolysaccharides. Biotechnol Adv 29: 54-66. doi: 10.1016/j.biotechadv.2010.08.011
    [11] Lebeer S, Vanderleyden J, De Keersmaecker SCJ (2008) Genes and molecules of Lactobacilli Supporting Probiotic Action. Microbiol Mol Biol Rev 72: 728-764. doi: 10.1128/MMBR.00017-08
    [12] Gauri DS, Mandal SM, Mondal K, et al. (2009) Enhanced production and partial characterization of an extracellular polysaccharide from newly isolated Azotobacter sp. SSB81. Bioresour Technol 100: 4240-4243. doi: 10.1016/j.biortech.2009.03.064
    [13] Marvasi M, Visscher P, Casillas-Martínez L (2010) Exopolymeric substances (EPS) from Bacillus subtilis: Polymers and genes encoding their synthesis. FEMS Microbiol Lett 313: 1-9. doi: 10.1111/j.1574-6968.2010.02085.x
    [14] Guchte M, Serror P, Chervaux C, et al. (2002) Stress response in lactic acid bacteria. Antonie van Leeuwenhoek 82: 187-216. doi: 10.1023/A:1020631532202
    [15] Papadimitriou K, Alegría Á, Bron PA, et al. (2016) Stress physiology of lactic acid bacteria. Microbiol Mol Biol Rev 80: 837-890. doi: 10.1128/MMBR.00076-15
    [16] Serrazanetti DI, Gottardi D, Montanari C, et al. (2013) Dynamic stresses of lactic acid bacteria associated to fermentation processes. Lactic Acid Bacteria–R & D for Food, Health and Livestock Purposes Rijeka: InTech, 539-570.
    [17] Riaz Rajoka MS, Wu Y, Mehwish HM, et al. (2020) Lactobacillus exopolysaccharides: New perspectives on engineering strategies, physiochemical functions, and immunomodulatory effects on host health. Trends Food Sci Technol 103: 36-48. doi: 10.1016/j.tifs.2020.06.003
    [18] van Hijum SAFT, Kralj S, Ozimek LK, et al. (2006) Structure-function relationships of glucansucrase and fructansucrase enzymes from lactic acid bacteria. Microbiol Mol Biol Rev 70: 157-176. doi: 10.1128/MMBR.70.1.157-176.2006
    [19] Galle S, Arendt E (2014) Exopolysaccharides from sourdough lactic acid bacteria. Crit Rev Food Sci Nutr 54: 891-901. doi: 10.1080/10408398.2011.617474
    [20] Zeidan AA, Poulsen VK, Janzen T, et al. (2017) Polysaccharide production by lactic acid bacteria: from genes to industrial applications. FEMS Microbiol Rev 41: S168-S200. doi: 10.1093/femsre/fux017
    [21] Laws A, Gu Y, Marshall V (2001) Biosynthesis, characterisation, and design of bacterial exopolysaccharides from lactic acid bacteria. Biotechnol Adv 19: 597-625. doi: 10.1016/S0734-9750(01)00084-2
    [22] Welman A, Maddox I (2003) Exopolysaccharides from lactic acid bacteria: Perspectives and challenges. Trends Biotechnol 21: 269-274. doi: 10.1016/S0167-7799(03)00107-0
    [23] Ruas-Madiedo P, Salazar N, de los Reyes-Gavilán CG (2009) Biosynthesis and chemical composition of exopolysaccharides produced by lactic acid bacteria. Bacterial Polysaccharides: Current Innovations and Future Trends Norwich: Caister Academic Press, 279-310.
    [24] Neves AR, Pool W, Kok J, et al. (2005) Overview on sugar metabolism and its control in–The input from in vivo NMR. FEMS Microbiol Rev 29: 531-554.
    [25] De Vuyst L, Degeest B (1999) Heteropolysaccharides from lactic acid bacteria. FEMS Microbiol Rev 23: 153-177. doi: 10.1016/S0168-6445(98)00042-4
    [26] Kleerebezem M, Hols P, Bernard E, et al. (2010) The extracellular biology of the Lactobacilli. FEMS Microbiol Rev 34: 199-230. doi: 10.1111/j.1574-6976.2009.00208.x
    [27] Looijesteijn PJ, Trapet L, Vries Ed, et al. (2001) Physiological function of exopolysaccharides produced by Lactococcus lactisInt J Food Microbiol 64: 71-80. doi: 10.1016/S0168-1605(00)00437-2
    [28] Ruas-Madiedo P, Hugenholtz J, Zoon P (2002) An overview of the functionality of exopolysaccharides produced by lactic acid bacteria. Int Dairy J 12: 163-171. doi: 10.1016/S0958-6946(01)00160-1
    [29] Caggianiello G, Kleerebezem M, Spano G (2016) Exopolysaccharides produced by lactic acid bacteria: from health-promoting benefits to stress tolerance mechanisms. Appl Microbiol Biotechnol 100: 3877-3886. doi: 10.1007/s00253-016-7471-2
    [30] Lee IC, Caggianiello G, Swam I, et al. (2016) Strain-specific features of extracellular polysaccharides and their impact on host interactions of Lactobacillus plantarumAppl Environ Microbiol 82: AEM.00306-00316.
    [31] Huu Thanh N, Razafindralambo H, Blecker C, et al. (2014) Stochastic exposure to sub-lethal high temperature enhances exopolysaccharides (EPS) excretion and improves Bifidobacterium bifidum cell survival to freeze-drying. Biochem Eng J 88: 85-94. doi: 10.1016/j.bej.2014.04.005
    [32] Desmond C, Stanton C, Fitzgerald GF, et al. (2002) Environmental adaptation of probiotic lactobacilli towards improvement of performance during spray drying. Int Dairy J 12: 183-190. doi: 10.1016/S0958-6946(02)00040-7
    [33] Donoghue H, Newman H (1976) Effect of glucose and sucrose on survival in batch culture of Streptococcus mutans C67-1 and a noncariogenic mutant, C67-25. Infect Immun 13: 16-21. doi: 10.1128/IAI.13.1.16-21.1976
    [34] Robijn G, Berg D, Haas H, et al. (1995) Determination of the structure of the exopolysaccharide produced by Lactobacillus sake 0–1. Carbohydr Res 276: 117-136. doi: 10.1016/0008-6215(95)00172-P
    [35] Robijn GW, Wienk HLJ, van den Berg DJC, et al. (1996) Structural studies of the exopolysaccharide produced by Lactobacillus paracasei 34-1. Carbohydr Res 285: 129-139. doi: 10.1016/S0008-6215(96)90178-0
    [36] Kitazawa H, Ishii Y, Uemura J, et al. (2000) Augmentation of macrophage functions by an extracellular phosphopolysaccharide from Lactobacillus delbrueckii ssp. bulgaricusFood Microbiol 17: 109-118. doi: 10.1006/fmic.1999.0294
    [37] Tallon R, Bressollier P, Urdaci MC (2003) Isolation and characterization of two exopolysaccharides produced by Lactobacillus plantarum EP56. Res Microbiol 154: 705-712. doi: 10.1016/j.resmic.2003.09.006
    [38] Waśko A, Polak-Berecka M, Gustaw W (2013) Increased viability of probiotic Lactobacillus rhamnosus after osmotic stress. Acta Aliment 42: 520-528. doi: 10.1556/AAlim.42.2013.4.7
    [39] Morales O, López-Cortés A, Hernandez-Duque G, et al. (2001) Extracellular polymers of microbial communities colonizing limestone surfaces. Methods Enzymol 336: 331-339. doi: 10.1016/S0076-6879(01)36599-0
    [40] Hill DR, Hladun Sl Fau-Scherer S, Scherer S Fau-Potts M, et al. (1994) Water stress proteins of Nostoc commune (Cyanobacteria) are secreted with UV-A/B-absorbing pigments and associate with 1,4-beta-D-xylanxylanohydrolase activity. J Biol Chem 269: 7726-7734.
    [41] Cotter P, Hill C (2003) Surviving the acid test: responses of gram-positive bacteria to low pH. Microbiol Mol Biol Rev 67: 429-453. doi: 10.1128/MMBR.67.3.429-453.2003
    [42] Chowdhury R, Sahu G, Das J (1996) Stress response in pathogenic bacteria. J Biosci 21: 149-160. doi: 10.1007/BF02703105
    [43] Ordax M, Marco-Noales E, López MM, et al. (2010) Exopolysaccharides favor the survival of Erwinia amylovora under copper stress through different strategies. Res Microbiol 161: 549-555. doi: 10.1016/j.resmic.2010.05.003
    [44] Yan M, Wang B-H, Xu X, et al. (2018) Extrusion of dissolved oxygen by exopolysaccharide from Leuconostoc mesenteroides and its implications in relief of the oxygen stress. Front Microbiol 9: 2467-2467. doi: 10.3389/fmicb.2018.02467
    [45] Zhang L, Liu C, Li D, et al. (2013) Antioxidant activity of an exopolysaccharide isolated from Lactobacillus plantarum C88. Int J Biol Macromol 54: 270-275. doi: 10.1016/j.ijbiomac.2012.12.037
    [46] Ruas-Madiedo P, de los Reyes-Gavilán CG (2005) Invited review: methods for the screening, isolation, and characterization of exopolysaccharides produced by lactic acid bacteria. J Dairy Sci 88: 843-856. doi: 10.3168/jds.S0022-0302(05)72750-8
    [47] Vurmaz M, Sahin E, Dertli E (2019) Potential Health Promoting Functions of Exopolysaccharides (EPS) from Lactic Acid Bacteria (LAB). 3rd International Conference on Advanced Engineering Technologies Bayburt: Bayburt University, 1379-1382.
    [48] Li H, Mao W, Hou Y, et al. (2012) Preparation, structure and anticoagulant activity of a low molecular weight fraction produced by mild acid hydrolysis of sulfated rhamnan from Monostroma latissimumBioresour Technol 114: 414-418. doi: 10.1016/j.biortech.2012.03.025
    [49] Li N, Liu X, He XX, et al. (2016) Structure and anticoagulant property of a sulfated polysaccharide isolated from the green seaweed Monostroma angicavaCarbohydr Polym 159.
    [50] Zhou Y, Cui Y, Qu X (2019) Exopolysaccharides of lactic acid bacteria: Structure, bioactivity and associations: A review. Carbohydr Polym 207: 317-332. doi: 10.1016/j.carbpol.2018.11.093
    [51] Abo Saif FAA, Sakr EAE (2020) Characterization and bioactivities of exopolysaccharide produced from probiotic Lactobacillus plantarum 47FE and Lactobacillus pentosus 68FE. Bioact Carbohydr Diet Fibre 24: 100231. doi: 10.1016/j.bcdf.2020.100231
    [52] Bello FD, Walter J, Hertel C, et al. (2001) In vitro study of prebiotic properties of levan-type exopolysaccharides from lactobacilli and non-digestible carbohydrates using denaturing gradient gel electrophoresis. Syst Appl Microbiol 24: 232-237. doi: 10.1078/0723-2020-00033
    [53] O'Connor EB, Barrett E, Fitzgerald G, et al. (2006) Production of vitamins, exopolysaccharides and bacteriocins by probiotic bacteria. Probiotic Dairy Products Hoboken: John Wiley & Sons Inc., 359-388.
    [54] Tsuda H, Miyamoto T (2010) Production of Exopolysaccharide by Lactobacillus plantarum and the Prebiotic Activity of the Exopolysaccharide. Food Sci Technol Res 16: 87-92. doi: 10.3136/fstr.16.87
    [55] Balzaretti S, Taverniti V, Guglielmetti S, et al. (2016) A novel rhamnose-rich hetero-exopolysaccharide isolated from Lactobacillus paracasei DG activates THP-1 human monocytic cells. Appl Environ Microbiol 83: e02702-02716.
    [56] Bengoa A, Llamas-Arriba M, Iraporda C, et al. (2017) Impact of growth temperature on exopolysaccharide production and probiotic properties of Lactobacillus paracasei strains isolated from kefir grains. Food Microbiol 69.
    [57] Das D, Baruah R, Goyal A (2014) A food additive with prebiotic properties of an alpha-D-glucan from Lactobacillus plantarum DM5. Int J Biol Macromol 69: 20-26. doi: 10.1016/j.ijbiomac.2014.05.029
    [58] Hongpattarakere T, Cherntong N, Wichienchot S, et al. (2012) In vitro prebiotic evaluation of exopolysaccharides produced by marine isolated lactic acid bacteria. Carbohydr Polym 87: 846-852. doi: 10.1016/j.carbpol.2011.08.085
    [59] Sasikumar K, Vaikkath D, Devendra L, et al. (2017) An exopolysaccharide (EPS) from a Lactobacillus plantarum BR2 with potential benefits for making functional foods. Bioresour Technol 241. doi: 10.1016/j.biortech.2017.05.075
    [60] Ishimwe N, Daliri E, Lee B, et al. (2015) The perspective on cholesterol lowering mechanisms of probiotics. Mol Nutr Food Res 59. doi: 10.1002/mnfr.201400548
    [61] Michael D, Davies T, Moss J, et al. (2017) The anti-cholesterolaemic effect of a consortium of probiotics: An acute study in C57BL/6J mice. Sci Rep 7: 2883. doi: 10.1038/s41598-017-02889-5
    [62] Rani RP, Anandharaj M, David Ravindran A (2018) Characterization of a novel exopolysaccharide produced by Lactobacillus gasseri FR4 and demonstration of its in vitro biological properties. Int J Biol Macromol 109: 772-783. doi: 10.1016/j.ijbiomac.2017.11.062
    [63] Pan D, Mei X (2010) Antioxidant activity of an exopolysaccharide purified from Lactococcus lactis subsp. lactis 12. Carbohydr Polym 80: 908-914. doi: 10.1016/j.carbpol.2010.01.005
    [64] Guo Y, Pan D, Li H, et al. (2013) Antioxidant and immunomodulatory activity of selenium exopolysaccharide produced by Lactococcus lactis subsp. lactisFood Chem 138: 84-89. doi: 10.1016/j.foodchem.2012.10.029
    [65] Saadat YR, Khosroushahi AY, Gargari BP (2019) A comprehensive review of anticancer, immunomodulatory and health beneficial effects of the lactic acid bacteria exopolysaccharides. Carbohydr Polym 217: 79-89. doi: 10.1016/j.carbpol.2019.04.025
    [66] Nurgali K, Jagoe RT, Abalo R (2018) Editorial: adverse effects of cancer chemotherapy: anything new to improve tolerance and reduce sequelae? Front Pharmacol 9: 245. doi: 10.3389/fphar.2018.00245
    [67] Wang K, Li W, Rui X, et al. (2014) Characterization of a novel exopolysaccharide with antitumor activity from Lactobacillus plantarum 70810. Int J Biol Macromol 63: 133-139. doi: 10.1016/j.ijbiomac.2013.10.036
    [68] Deepak V, Ramachandran S, Balahmar RM, et al. (2016) In vitro evaluation of anticancer properties of exopolysaccharides from Lactobacillus acidophilus in colon cancer cell lines. In Vitro Cell Dev Biol Anim 52: 163-173. doi: 10.1007/s11626-015-9970-3
    [69] Riaz Rajoka MS, Mehwish HM, Zhang H, et al. (2020) Antibacterial and antioxidant activity of exopolysaccharide mediated silver nanoparticle synthesized by Lactobacillus brevis isolated from Chinese koumiss. Colloids Surf B 186: 110734. doi: 10.1016/j.colsurfb.2019.110734
    [70] Kim K, Lee G, Thanh HD, et al. (2018) Exopolysaccharide from Lactobacillus plantarum LRCC5310 offers protection against rotavirus-induced diarrhea and regulates inflammatory response. J Dairy Sci 101: 5702-5712. doi: 10.3168/jds.2017-14151
    [71] Gaucher F, Bonnassie S, Rabah H, et al. (2019) Review: adaptation of beneficial propionibacteria, lactobacilli, and bifidobacteria improves tolerance toward technological and digestive stresses. Front Microbiol 10: 841. doi: 10.3389/fmicb.2019.00841
    [72] Phillips KN, Godwin CM, Cotner JB (2017) The effects of nutrient imbalances and temperature on the biomass stoichiometry of freshwater bacteria. Front Microbiol 8: 1692. doi: 10.3389/fmicb.2017.01692
    [73] Adebayo-Tayo BC, Onilude AO (2008) Comparative influence of medium composition on biomassgrowth, lactic acid and exopolysaccharides production bysome strains of lactic acid bacteria. The Internet J Microbiol 7.
    [74] Mbye M, Baig MA, AbuQamar SF, et al. (2020) Updates on understanding of probiotic lactic acid bacteria responses to environmental stresses and highlights on proteomic analyses. Compr Rev Food Sci Food Saf 19: 1110-1124. doi: 10.1111/1541-4337.12554
    [75] Cirrincione S, Breuer Y, Mangiapane E, et al. (2018) ‘Ropy’ phenotype, exopolysaccharides and metabolism: Study on food isolated potential probiotics LAB. Microbiol Res 214: 137-145. doi: 10.1016/j.micres.2018.07.004
    [76] Ninomiya K, Matsuda K, Kawahata T, et al. (2009) Effect of CO2 concentration on the growth and exopolysaccharide production of Bifidobacterium longum cultivated under anaerobic conditions. J Biosci Bioeng 107: 535-537. doi: 10.1016/j.jbiosc.2008.12.015
    [77] Marshall VM, Cowie EN, Moreton RS (2009) Analysis and production of two exopolysaccharides from Lactococcus lactis subsp. cremoris LC330. J Dairy Res 62: 621-628. doi: 10.1017/S0022029900031356
    [78] García-Garibay M, Marshall V (2008) Polymer production by Lactobacillus delbrueckii ssp. J Appl Microbiol 70: 325-328.
    [79] Seesuriyachan P, Kuntiya A, Hanmoungjai P, et al. (2012) Optimization of exopolysaccharide overproduction by Lactobacillus confusus in solid state fermentation under high salinity stress. Biosci Biotechnol Biochem 76: 912-917. doi: 10.1271/bbb.110905
    [80] Hussein M-D, Ghaly M, Osman M, et al. (2015) Production and prebiotic activity of exopolysaccharides derived from some probiotics. Egypt Pharm J 14: 1-9. doi: 10.4103/1687-4315.154687
    [81] Korakli M, Pavlovic M, Vogel R (2003) Exopolysaccharide and kestose production by Lactobacillus sanfranciscensis LTH2590. Appl Environ Microbiol 69: 2073-2079. doi: 10.1128/AEM.69.4.2073-2079.2003
    [82] Dols M, Remaud-Simeon M, Monsan PF (1997) Dextransucrase production by Leuconostoc mesenteroides NRRL B-1299. Comparison with L. mesenteroides NRRL B-512F. Enzyme Microb Technol 20: 523-530. doi: 10.1016/S0141-0229(96)00189-5
    [83] Yuksekdag ZN, Aslim B (2008) Influence of different carbon sources on exopolysaccharide production by Lactobacillus delbrueckii subsp. bulgaricus (B3, G12) and Streptococcus thermophilus (W22). Braz Arch Biol Technol 51: 581-585. doi: 10.1590/S1516-89132008000300019
    [84] Cerning J, Renard C, Thibault J, et al. (1994) Carbon source requirements for exopolysaccharide production by Lactobacillus casei CG11 and partial structure analysis of the polymer. Appl Environ Microbiol 60: 3914-3919. doi: 10.1128/AEM.60.11.3914-3919.1994
    [85] Gamar L, Blondeau K, Simonet JM (2003) Physiological approach to extracellular polysaccharide production by Lactobacillus rhamnosus strain C83. J Appl Microbiol 83: 281-287. doi: 10.1046/j.1365-2672.1997.00228.x
    [86] Arsène-Ploetze F, Bringel F (2004) Role of inorganic carbon in lactic acid bacteria metabolism.84: 49-59.
    [87] Arioli S, Roncada P, Salzano AM, et al. (2009) The relevance of carbon dioxide metabolism in Streptococcus thermophilusMicrobiology 155: 1953-1965. doi: 10.1099/mic.0.024737-0
    [88] Ninomiya K, Matsuda K, Kawahata T, et al. (2009) Effect of CO2 concentration on the growth and exopolysaccharide production of Bifidobacterium longum cultivated under anaerobic conditions. J Biosci Bioeng 107: 535-537. doi: 10.1016/j.jbiosc.2008.12.015
    [89] Santillan EF, Shanahan T, Omelon C, et al. (2015) Isolation and characterization of a CO2-tolerant Lactobacillus strain from Crystal Geyser, Utah, U.S.A. Front Earth Sci 3: 41.
    [90] Golowczyc M, Silva J, Teixeira P, et al. (2011) Cellular injuries of spray-dried Lactobacillus spp. isolated from kefir and their impact on probiotic properties. Int J Food Microbiol 144: 556-560. doi: 10.1016/j.ijfoodmicro.2010.11.005
    [91] Qian Y, Borowski WJ, Calhoon WD (2011) Intracellular granule formation in response to oxidative stress in BifidobacteriumInt J Food Microbiol 145: 320-325. doi: 10.1016/j.ijfoodmicro.2010.11.026
    [92] Amund D, Ouoba L, Sutherland J, et al. (2014) Assessing the effects of exposure to environmental stress on some functional properties of Bifidobacterium animalis ssp. lactisBenefi Microbes 5: 1-9. doi: 10.3920/BM2013.0099
    [93] Donlan R (2002) Biofilms: Microbial Life on Surfaces. Emerging Infect Dis 8: 881-890. doi: 10.3201/eid0809.020063
    [94] Flemming H-C, Wingender J (2001) Relevance of microbial extracellular polymeric substances (EPSs) - Part I: Structural and ecological aspects. Water Sci Technol 43: 1-8. doi: 10.2166/wst.2001.0326
    [95] Ciszek-Lenda M (2011) Biological functions of exopolysaccharides from probiotic bacteria. Cent Eur J Immun 36: 51-55.
    [96] Lebeer S, Verhoeven T, Velez M, et al. (2007) Impact of environmental and genetic factors on biofilm formation by the probiotic strain Lactobacillus rhamnosus GG. Appl Environ Microbiol 73: 6768-6775. doi: 10.1128/AEM.01393-07
    [97] Slížová M, Nemcova R, Madar M, et al. (2015) Analysis of biofilm formation by intestinal lactobacilli. Can J Microbiol 61: 1-10. doi: 10.1139/cjm-2015-0007
    [98] Torino MI, Hébert EM, Mozzi F, et al. (2005) Growth and exopolysaccharide production by Lactobacillus helveticus ATCC 15807 in an adenine-supplemented chemically defined medium. J Appl Microbiol 99: 1123-1129. doi: 10.1111/j.1365-2672.2005.02701.x
    [99] Sanhueza Carrera E, Paredes-Osses E, González C, et al. (2015) Effect of pH in the survival of Lactobacillus salivarius strain UCO_979C wild type and the pH acid acclimated variant. Electron J Biotechnol 18: 343-346. doi: 10.1016/j.ejbt.2015.06.005
    [100] Grosu-Tudor SS, Zamfir M (2014) Exopolysaccharide production by selected lactic acid bacteria isolated from fermented vegetables. Sci Bulletin Series F Biotechnol 18: 107-114.
    [101] Ananta E, Volkert M, Knorr D (2005) Cellular injuries and storage stability of spray-dried Lactobacillus rhamnosus GG. Int Dairy J 15: 399-409. doi: 10.1016/j.idairyj.2004.08.004
    [102] Nguyen HT, Truong DH, Kouhounde S, et al. (2016) Biochemical engineering approaches for increasing viability and functionality of probiotic bacteria. Int J Mol Sci 17. doi: 10.3390/ijms17060867
    [103] Bader J, Mast-Gerlach E, Popović M, et al. (2010) Relevance of microbial coculture fermentations in biotechnology. J Appl Microbiol 109: 371-387. doi: 10.1111/j.1365-2672.2009.04659.x
    [104] Smid E, Lacroix C (2012) Microbe-microbe interactions in mixed culture food fermentations. Curr Opin Biotechnol 24.
    [105] Tada S, Katakura Y, Ninomiya K, et al. (2007) Fed-Batch coculture of Lactobacillus kefiranofaciens with Saccharomyces cerevisiae for effective production of kefiran. J Biosci Bioeng 103: 557-562. doi: 10.1263/jbb.103.557
    [106] Bertsch A, Roy D, LaPointe G (2019) Enhanced exopolysaccharide production by Lactobacillus rhamnosus in co-culture with Saccharomyces cerevisiaeAppl Sci 9: 4026. doi: 10.3390/app9194026
    [107] Yamasaki-Yashiki S, Sawada H, Kino-oka M, et al. (2016) Analysis of gene expression profiles of Lactobacillus Paracasei induced by direct contact with Saccharomyces Cerevisiae through recognition of yeast mannan. Biosci Microbiota Food Health 36.
    [108] Zhang X, Li Z, Pang S, et al. (2020) The impact of cell structure, metabolism and group behavior for the survival of bacteria under stress conditions. Arch Microbiol .
    [109] Jin J, Zhang B, Guo H, et al. (2012) Mechanism analysis of acid tolerance response of Bifidobacterium longum subsp. longum BBMN 68 by gene expression profile using RNA-sequencing. PLOS One 7: e50777. doi: 10.1371/journal.pone.0050777
    [110] Rasulov BA, Dai J, Pattaeva MA, et al. (2020) Gene expression abundance dictated exopolysaccharide modification in Rhizobium radiobacter SZ4S7S14 as the cell's response to salt stress. Int J Biol Macromol 164: 4339-4347. doi: 10.1016/j.ijbiomac.2020.09.038
    [111] Ruas-Madiedo P, Gueimonde M, Arigoni F, et al. (2009) Bile affects the synthesis of exopolysaccharides by Bifidobacterium animalisAppl Environ Microbiol 75: 1204-1207. doi: 10.1128/AEM.00908-08
    [112] Wu Q, Shah NP (2018) Comparative mRNA-Seq analysis reveals the improved EPS production machinery in Streptococcus thermophilus ASCC 1275 during optimized milk fermentation. Front Microbiol 9: 445. doi: 10.3389/fmicb.2018.00445
    [113] Stack H, Kearney N, Stanton C, et al. (2010) Association of beta-glucan endogenous production with increased stress tolerance of intestinal lactobacilli. Appl Environ Microbiol 76: 500-507. doi: 10.1128/AEM.01524-09
    [114] Guo W, Gao J, Wang HJ, et al. (2020) Phosphoglycerate kinase is involved in carbohydrate utilization, extracellular polysaccharide biosynthesis, and cell motility of Xanthomonas axonopodis pv. glycines independent of Clp. Front Microbiol 11: 91. doi: 10.3389/fmicb.2020.00091
    [115] Prasad J, McJarrow P, Gopal P (2003) Heat and osmotic stress responses of probiotic Lactobacillus rhamnosus HN001 (DR20) in relation to viability after drying. Appl Environ Microbiol 69: 917-925. doi: 10.1128/AEM.69.2.917-925.2003
    [116] Xu Y, Cui Y, Yue F, et al. (2019) Exopolysaccharides produced by lactic acid bacteria and Bifidobacteria: Structures, physiochemical functions and applications in the food industry. Food Hydrocolloids 94: 475-499. doi: 10.1016/j.foodhyd.2019.03.032
    [117] Wang Q, Wang F, Xu Z, et al. (2017) Bioactive mushroom polysaccharides: a review on monosaccharide composition, biosynthesis and regulation. Molecules 22.
    [118] Chen YC, Wu YJ, Hu CY (2019) Monosaccharide composition influence and immunomodulatory effects of probiotic exopolysaccharides. Int J Biol Macromol 133: 575-582. doi: 10.1016/j.ijbiomac.2019.04.109
    [119] Kumar AS, Mody K, Jha B (2007) Bacterial exopolysaccharides-a perception. J Basic Microbiol 47: 103-117. doi: 10.1002/jobm.200610203
  • Reader Comments
  • © 2020 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)
通讯作者: 陈斌, bchen63@163.com
  • 1. 

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索

Metrics

Article views(10852) PDF downloads(807) Cited by(48)

Article outline

Figures and Tables

Figures(5)  /  Tables(1)

/

DownLoad:  Full-Size Img  PowerPoint
Return
Return

Catalog