Abstract
The exopolysaccharides (EPSs) of lactic acid bacteria (LAB) have presented various bioactivities and beneficial characteristics, rendering their vast commercial value and attracting a broad interest of researchers. The diversity of EPS structures contributes to the changes of EPS functions. However, the low yield of EPS of LAB has severely limited these biopolymers’ comprehensive studies and applications in different areas, such as functional food, health and medicine fields. The clarification of biosynthesis mechanism of EPS will accelerate the synthesis and reconstruction of EPS. In recent years, with the development of new genetic manipulation techniques, there has been significant progress in the EPS biosynthesis mechanisms in LAB. In this review, the structure of LAB-derived EPSs, the EPS biosynthesis basic pathways in LAB, the EPS biosynthetic gene cluster, and the regulation mechanism of EPS biosynthesis will be summarized. It will focus on the latest progress in EPS biosynthesis regulation of LAB and provide prospects for future related developments.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data reported in this review are available in the correspondingly cited articles.
References
Abarquero D, Renes E, Fresno JM, Tornadijo ME (2022) Study of exopolysaccharides from lactic acid bacteria and their industrial applications: a review. Int J Food Sci Technol 57:16–26. https://doi.org/10.1111/ijfs.15227
Ai LZ, Guo QB, Ding HH, Guo BH, Chen W, Cui SW (2016) Structure characterization of exopolysaccharides from Lactobacillus casei LC2W from skim milk. Food Hydrocolloid 56:134–143. https://doi.org/10.1016/j.foodhyd.2015.10.023
Andersen JM, Barrangou R, Abou Hachem M, Lahtinen S, Goh YJ, Svensson B, Klaenhammer TR (2011) Transcriptional and functional analysis of galactooligosaccharide uptake by lacS in Lactobacillus acidophilus. Proc Natl Acad Sci U S A 108(43):17785–17790. https://doi.org/10.1073/pnas.1114152108
Angelin J, Kavitha M (2020) Exopolysaccharides from probiotic bacteria and their health potential. Int J Biol Macromol 162:853–865. https://doi.org/10.1016/j.ijbiomac.2020.06.190
Anwar MA, Kralj S, van der Maarel MJ, Dijkhuizen L (2008) The probiotic Lactobacillus johnsonii NCC 533 produces high-molecular-mass inulin from sucrose by using an inulosucrase enzyme. Appl Environ Microbiol 74(11):3426–3433. https://doi.org/10.1128/AEM.00377-08
Anwar MA, Kralj S, Piqué AV, Leemhuis H, van der Maarel MJEC, Dijkhuizen L (2010) Inulin and levan synthesis by probiotic Lactobacillus gasseri strains: characterization of three novel fructansucrase enzymes and their fructan products. Microbiology 156(Pt 4):1264–1274. https://doi.org/10.1099/mic.0.036616-0
Ayyash M, Abu-Jdayil B, Olaimat A, Esposito G, Itsaranuwat P, Osaili T, Obaid R, Kizhakkayil J, Liu SQ (2020) Physicochemical, bioactive and rheological properties of an exopolysaccharide produced by a probiotic Pediococcus pentosaceus M41. Carbohydr Polym 229:115462. https://doi.org/10.1016/j.carbpol.2019.115462
Balzaretti S, Taverniti V, Guglielmetti S, Fiore W, Minuzzo M, Ngo HN, Ngere JB, Sadiq S, Humphreys PN, Laws AP (2017) A novel rhamnose-rich hetero-exopolysaccharideisolated from Lactobacillus paracasei DG activates THP-1 human monocytic cells. Appl Environ Microbiol 83(3):e02702–e02716. https://doi.org/10.1128/AEM.02702-16
Biswas S, Biswas I (2006) Regulation of the glucosyltransferase (gtfBC) operon by CovR in Streptococcus mutans. J Bacteriol 188(3):988–998. https://doi.org/10.1128/JB.188.3.988-998.2006
Brown R, Marchesi JR, Morby AP (2011) Functional characterisation of Lp_2714, an EAL-domain protein from Lactobacillus plantarum. Biochem Biophys Res Commun 411(1):132–136. https://doi.org/10.1016/j.bbrc.2011.06.112
Cao F, Liang M, Liu J, Liu Y, Renye JA Jr, Qi PX, Ren D (2021) Characterization of an exopolysaccharide (EPS-3A) produced by Streptococcus thermophilus ZJUIDS-2-01 isolated from traditional yak yogurt. Int J Biol Macromol 192:1331–1343. https://doi.org/10.1016/j.ijbiomac.2021.10.055
Charoenwongpaiboon T, Wangpaiboon K, Pichyangkura R, Nepogodiev SA, Wonganan P, Mahalapbutr P, Field RA (2021) Characterization of a nanoparticulate exopolysaccharide from Leuconostoc holzapfelii KM01 and its potential application in drug encapsulation. Int J Biol Macromol 187:690–698. https://doi.org/10.1016/j.ijbiomac.2021.07.174
Chen L, Li X, Zhou X, Zeng J, Ren Z, Lei L, Kang D, Zhang K, Zou J, Li Y (2018) Inhibition of Enterococcus faecalis growth and biofilm formation by molecule targeting cyclic di-AMP synthetase activity. J Endod 44(9):1381–1388e2. https://doi.org/10.1016/j.joen.2018.05.008
Cheng X, Zheng X, Zhou X, Zeng J, Ren Z, Xu X, Cheng L, Li M, Li J, Li Y (2016) Regulation of oxidative response and extracellular polysaccharide synthesis by a diadenylate cyclase in Streptococcus mutans. Environ Microbiol 18(3):904–922. https://doi.org/10.1111/1462-2920.13123
Colton DM, Stabb EV (2016) Rethinking the roles of CRP, cAMP, and sugar-mediated global regulation in the Vibrionaceae. Curr Genet 62(1):39–45. https://doi.org/10.1007/s00294-015-0508-8
Colton DM, Stoudenmire JL, Stabb EV (2015) Growth on glucose decreases cAMP-CRP activity while paradoxically increasing intracellular cAMP in the light-organ symbiont Vibrio fischeri. Mol Microbiol 97(6):1114–1127. https://doi.org/10.1111/mmi.13087
Côté GL, Skory CD (2012) Cloning, expression, and characterization of an insoluble glucan-producing glucansucrase from Leuconostoc mesenteroides NRRL B-1118. Appl Microbiol Biotechnol 93(6):2387–2394. https://doi.org/10.1007/s00253-011-3562-2
Cui Y, Qu X (2021) Genetic mechanisms of prebiotic carbohydrate metabolism in lactic acid bacteria: emphasis on lacticaseibacillus casei and lacticaseibacillus paracasei as flexible, diverse and outstanding prebiotic carbohydrate starters. Trends Food Sci Tech 115:486–499. https://doi.org/10.1016/j.tifs.2021.06.058
Cui Y, Jiang X, Hao M, Qu X, Hu T (2017) New advances in exopolysaccharides production of Streptococcus thermophilus. Arch Microbiol 199(6):799–809. https://doi.org/10.1007/s00203-017-1366-1
Cui Y, Wang M, Zheng Y, Miao K, Qu X (2021) The Carbohydrate metabolism of lactiplantibacillus plantarum. Int J Mol Sci 22(24):13452. https://doi.org/10.3390/ijms222413452
Cuthbertson L, Mainprize IL, Naismith JH, Whitfield C (2009) Pivotal roles of the outer membrane polysaccharide export and polysaccharide copolymerase protein families in export of extracellular polysaccharides in Gram-negative bacteria. Microbiol Mol Biol Rev 73(1):155–177. https://doi.org/10.1128/MMBR.00024-08
Davidson AL, Dassa E, Orelle C, Chen J (2008) Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol Rev 72(2):317–364. https://doi.org/10.1128/MMBR.00031-07
De Filippis F, Pasolli E, Ercolini D (2020) The food-gut axis: lactic acid bacteria and their link to food, the gut microbiome and human health. FEMS Microbiol Rev 44(4):454–489. https://doi.org/10.1093/femsre/fuaa015
Dertli E, Mayer MJ, Colquhoun IJ, Narbad A (2016) EpsA is an essential gene in exopolysaccharide production in Lactobacillus johnsonii FI9785. Microb Biotechnol 9(4):496–501. https://doi.org/10.1111/1751-7915.12314
Deutscher J, Francke C, Postma PW (2006) How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol Mol Biol Rev 70(4):939–1031. https://doi.org/10.1128/MMBR.00024-06
Du R, Pei F, Kang J, Zhang W, Wang S, Ping W, Ling H, Ge J (2022) Analysis of the structure and properties of dextran produced by Weissella confusa. Int J Biol Macromol 204:677–684. https://doi.org/10.1016/j.ijbiomac.2022.02.038
Feng X, Zhang H, Lai PFH, Xiong Z, Ai L (2021) Structure characterization of a pyruvated exopolysaccharide from Lactobacillus plantarum AR307. Int J Biol Macromol 178:113–120. https://doi.org/10.1016/j.ijbiomac.2021.02.119
Freitas F, Alves VD, Reis MA (2011) Advances in bacterial exopolysaccharides: from production to biotechnological applications. Trends Biotechnol 29(8):388–398. https://doi.org/10.1016/j.tibtech.2011.03.008
Goh KK, Haisman DR, Singh H (2005) Development of an improved procedure for isolation and purification of exopolysaccharides produced by Lactobacillus delbrueckii subsp. bulgaricus NCFB 2483. Appl Microbiol Biotechnol 67(2):202–208. https://doi.org/10.1007/s00253-004-1739-7
Guan Y, Cui Y, Wang Q, Qu X (2023) Inulin increases the EPS biosynthesis of Lactobacillus delbrueckii ssp. bulgaricus LDB-C1. Biotechnol Lett 45(5–6):639–654. https://doi.org/10.1007/s10529-023-03365-z
Gundlach J, Rath H, Herzberg C, Mader U, Stulke J (2016) Second messenger signaling in Bacillus subtilis: accumulation of cyclic di-AMP inhibits biofilm formation. Front Microbiol 7:804. https://doi.org/10.3389/fmicb.2016.00804
He J, Ruan W, Sun J, Wang F, Yan W (2018) Functional characterization of c-di-GMP signaling-related genes in the probiotic Lactobacillus acidophilus. Front Microbiol 9:1935. https://doi.org/10.3389/fmicb.2018.01935
Hu SM, Zhou JM, Zhou QQ, Li P, Xie YY, Zhou T, Gu P (2021) Purification, characterization and biological activities of exopolysaccharides from Lactobacillus rhamnosus ZFM231 isolated from milk. LWT-Food Sci Techonl 147:111561. https://doi.org/10.1016/j.lwt.2021.111561
Iskandar CF, Cailliez-Grimal C, Borges F, Revol-Junelles AM (2019) Review of lactose and galactose metabolism in lactic acid bacteria dedicated to expert genomic annotation. Trends Food Sci Tech 88:121–132. https://doi.org/10.1016/j.tifs.2019.03.020
Jiang YY, Yang ZN (2018) A functional and genetic overview of exopolysaccharides produced by Lactobacillus plantarum. J Funct Foods 47:229–240. https://doi.org/10.1016/j.jff.2018.05.060
Jolly L, Stingele F (2001) Molecular organization and functionality of exopolysaccharide gene clusters in lactic acid bacteria. Int Dairy J 11:733–745. https://doi.org/10.1016/S0958-6946(01)00117-0
Jurášková D, Ribeiro SC, Silva CCG (2022) Exopolysaccharides produced by lactic acid bacteria: from biosynthesis to health-promoting properties. Foods 11(2):156. https://doi.org/10.3390/foods11020156
Kanamarlapudi SLRK, Muddada S (2017) Characterization of exopolysaccharide produced by Streptococcus thermophilus CC30. Biomed Res Int 2017:4201809. https://doi.org/10.1155/2017/4201809
Kavitake D, Devi PB, Singh SP, Shetty PH (2016) Characterization of a novel galactan produced by Weissella confusa KR780676 from an acidic fermented food. Int J Biol Macromol 86:681–689. https://doi.org/10.1016/j.ijbiomac.2016.01.099
Kong L, Huang Y, Zeng X, Ye C, Wu Z, Guo Y, Pan D (2022a) Effects of galactosyltransferase on EPS biosynthesis and freeze-drying resistance of Lactobacillus acidophilus NCFM. Food Chem (Oxf) 5:100145. https://doi.org/10.1016/j.fochms.2022.100145
Kong L, Song X, Xia Y, Ai L, Xiong Z (2022b) Construction of a CRISPR/nCas9-assisted genome editing system for exopolysaccharide biosynthesis in Streptococcus thermophilus. Food Res Int 158:111550. https://doi.org/10.1016/j.foodres.2022.111550
Krol E, Werel L, Essen LO, Becker A (2023) Structural and functional diversity of bacterial cyclic nucleotide perception by CRP proteins. Microlife 4:uqad024. https://doi.org/10.1093/femsml/uqad024
Lakra AK, Domdi L, Tilwani YM, Arul V (2020) Physicochemical and functional characterization of mannan exopolysaccharide from Weissella confusa MD1 with bioactivities. Int J Biol Macromol 143:797–805. https://doi.org/10.1016/j.ijbiomac.2019.09.139
Lebeer S, Verhoeven TL, Francius G, Schoofs G, Lambrichts I, Dufrene Y, Vanderleyden J, De Keersmaecker SC (2009) Identification of a gene cluster for the biosynthesis of a long, galactose-rich exopolysaccharide in Lactobacillus rhamnosus GG and functional analysis of the priming glycosyltransferase. Appl Environ Microbiol 75:3554–3563. https://doi.org/10.1128/AEM.02919-08
Lee IC, Caggianiello G, van Swam II, Taverne N, Meijerink M, Bron PA, Spano G, Kleerebezem M (2016) Strain-specific features of extracellular polysaccharides and their impact on Lactobacillus plantarum-host interactions. Appl Environ Microbiol 82(13):3959–3970. https://doi.org/10.1128/AEM.00306-16
Li C, Sun JW, Zhang GF, Liu LB (2016) Effect of the absence of the CcpA gene on growth, metabolic production, and stress tolerance in Lactobacillus delbrueckii ssp. bulgaricus. J Dairy Sci 99(1):104–111. https://doi.org/10.3168/jds.2015-10321
Li Y, Liu Y, Cao C, Zhu X, Wang C, Wu R, Wu J (2020) Extraction and biological activity of exopolysaccharide produced by Leuconostoc mesenteroides SN-8. Int J Biol Macromol 157:36–44. https://doi.org/10.1016/j.ijbiomac.2020.04.150
Mayer MJ, D’Amato A, Colquhoun IJ, Le Gall G, Narbad A (2020) Identification of genes required for glucan exopolysaccharide production in Lactobacillus johnsonii suggests a novel biosynthesis mechanism. Appl Environ Microbiol 86(8):e02808–e02819. https://doi.org/10.1128/AEM.02808-19
Mazzeo MF, Cacace G, Peluso A, Zotta T, Muscariello L, Vastano V, Parente E, Siciliano RA (2012) Effect of inactivation of ccpA and aerobic growth in Lactobacillus plantarum: a proteomic perspective. J Proteom 75(13):4050–4061. https://doi.org/10.1016/j.jprot.2012.05.019
Meng F, Lyu Y, Chen X, Lu F, Zhao H, Lu Y, Zhao M, Lu Z (2023a) Maltose-enhanced exopolysaccharide synthesis of lactiplantibacillus plantarum through CRP-like protein. J Agric Food Chem 71(2):1113–1121. https://doi.org/10.1021/acs.jafc.2c07880
Meng F, Lyu Y, Zhao H, Lyu F, Bie X, Lu Y, Zhao M, Chen Y, Lu Z (2023b) LsrR-like protein responds to stress tolerance by regulating polysaccharide biosynthesis in lactiplantibacillus plantarum. Int J Biol Macromol 225:1193–1203. https://doi.org/10.1016/j.ijbiomac.2022.11.180
Moradi Z, Kalanpour N (2019) Kefiran, a branched polysaccharide: Preparation, properties and applications: a review. Carbohydr Polym 223:115100. https://doi.org/10.1016/j.carbpol.2019.115100
Morona R, Purins L, Tocilj A, Matte A, Cygler M (2009) Sequence-structure relationships in polysaccharide co-polymerase (PCP) proteins. Trends Biochem Sci 34:78–84. https://doi.org/10.1016/j.tibs.2008.11.001
Muscariello L, Marasco R, De Felice M, Sacco M (2001) The functional ccpA gene is required for carbon catabolite repression in Lactobacillus plantarum. Appl Environ Microbiol 67(7):2903–2907. https://doi.org/10.1128/AEM.67.7.2903-2907.2001
Muscariello L, Marino C, Capri U, Vastano V, Marasco R, Sacco M (2013) CcpA and three newly identified proteins are involved in biofilm development in Lactobacillus plantarum. J Basic Microbiol 53(1):62–71. https://doi.org/10.1002/jobm.201100456
Ni D, Xu W, Bai Y, Zhang W, Zhang T, Mu W (2018a) Biosynthesis of levan from sucrose using a thermostable levansucrase from Lactobacillus reuteri LTH5448. Int J Biol Macromol 113:29–37. https://doi.org/10.1016/j.ijbiomac.2018.01.187
Ni D, Zhu Y, Xu W, Bai Y, Zhang T, Mu W (2018b) Biosynthesis of inulin from sucrose using inulosucrase from Lactobacillus gasseri DSM 20604. Int J Biol Macromol 109:1209–1218. https://doi.org/10.1016/j.ijbiomac.2017.11.120
Noda M, Sugimoto S, Hayashi I, Danshiitsoodol N, Fukamachi M, Sugiyama M (2018) A novel structure of exopolysaccharide produced by a plant-derived lactic acid bacterium Lactobacillus paracasei IJH-SONE68. J Biochem 164(2):87–92. https://doi.org/10.1093/jb/mvy048
Olvera C, Centeno-Leija S, López-Munguía A (2007) Structural and functional features of fructansucrases present in Leuconostoc mesenteroides ATCC 8293. Antonie Van Leeuwenhoek 92(1):11–20. https://doi.org/10.1007/s10482-006-9128-0
Pachekrepapol U, Lucey JA, Gong Y, Naran R, Azadi P (2017) Characterization of the chemical structures and physical properties of exopolysaccharides produced by various Streptococcus thermophilus strains. J Dairy Sci 100(5):3424–3435. https://doi.org/10.3168/jds.2016-12125
Padmanabhan A, Shah NP (2020) Structural characterization of exopolysaccharide from Streptococcus thermophilus ASCC 1275. J Dairy Sci 103(8):6830–6842. https://doi.org/10.3168/jds.2019-17439
Padmanabhan A, Tong Y, Wu Q, Zhang J, Shah NP (2018) Transcriptomic insights into the growth phase- and sugar-associated changes in the exopolysaccharide production of a high EPS-producing Streptococcus thermophilus ASCC 1275. Front Microbiol 9:1919. https://doi.org/10.3389/fmicb.2018.01919
Peng X, Zhang Y, Bai G, Zhou X, Wu H (2016) Cyclic di-AMP mediates biofilm formation. Mol Microbiol 99(5):945–959. https://doi.org/10.1111/mmi.13277
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. https://doi.org/10.1016/j.ijbiomac.2017.11.062
Ravcheev DA, Khoroshkin MS, Laikova ON, Tsoy OV, Sernova NV, Petrova SA, Rakhmaninova AB, Novichkov PS, Gelfand MS, Rodionov DA (2014) Comparative genomics and evolution of regulons of the LacI-family transcription factors. Front Microbiol 5:294. https://doi.org/10.3389/fmicb.2014.00294
Rehm BH (2010) Bacterial polymers: biosynthesis, modifications and applications. Nat Rev Microbiol 8:578–592. https://doi.org/10.1038/nrmicro2354
Remus DM, van Kranenburg R, van Swam II, Taverne N, Bongers RS, Wels M, Wells JM, Bron PA, Kleerebezem M (2012) Impact of 4 Lactobacillus plantarum capsular polysaccharide clusters on surface glycan composition and host cell signaling. Microb Cell Fact 11:149. https://doi.org/10.1186/1475-2859-11-149
Ren W, Xia Y, Wang G, Zhang H, Zhu S, Ai L (2016) Bioactive exopolysaccharides from a Sthermophilus strain: screening purification and characterization. Int J Biol Macromol 86:402–407. https://doi.org/10.1016/j.ijbiomac.2016.01.085
Ricciardi A, Parente E, Crudele MA, Zanetti F, Scolari G, Mannazzu I (2002) Exopolysaccharide production by Streptococcus thermophilus SY: production and preliminary characterization of the polymer. J Appl Microbiol 92(2):297–306. https://doi.org/10.1046/j.1365-2672.2002.01487.x
Ritzert JT, Minasov G, Embry R, Schipma MJ, Satchell KJF (2019) The cyclic AMP receptor protein regulates quorum sensing and global gene expression in Yersinia pestis during planktonic growth and growth in biofilms. mBio 10(6):e02613–e02619. https://doi.org/10.1128/mBio.02613-19
Ruffing A, Chen RR (2006) Metabolic engineering of microbes for oligosaccharide and polysaccharide synthesis. Microb Cell Fact 5:25. https://doi.org/10.1186/1475-2859-5-25
Salimi F, Farrokh P (2023) Recent advances in the biological activities of microbial exopolysaccharides. World J Microbiol Biotechnol 39(8):213. https://doi.org/10.1007/s11274-023-03660-x
Şanlier N, Gökcen BB, Sezgin AC (2019) Health benefits of fermented foods. Crit Rev Food Sci Nutr 59(3):506–527. https://doi.org/10.1080/10408398.2017.1383355
Schmid J, Sieber V, Rehm B (2015) Bacterial exopolysaccharides: biosynthesis pathways and engineering strategies. Front Microbiol 6:496. https://doi.org/10.3389/fmicb.2015.00496
Song X, Xiong Z, Kong L, Wang G, Ai L (2018) Relationship between putative eps genes and production of exopolysaccharide in Lactobacillus casei LC2W. Front Microbiol 9:1882. https://doi.org/10.3389/fmicb.2018.01882
Soumya MP, Nampoothiri KM (2021) An overview of functional genomics and relevance of glycosyltransferases in exopolysaccharide production by lactic acid bacteria. Int J Biol Macromol 184:1014–1025. https://doi.org/10.1016/j.ijbiomac.2021.06.131
Sun N, Liu H, Liu S, Zhang X, Chen P, Li W, Xu X, Tian W (2018) Purification, preliminary structure and antitumor activity of exopolysaccharide produced by Streptococcus thermophilus CH9. Molecules 23(11):2898. https://doi.org/10.3390/molecules23112898
Tang WZ, Dong MS, Wang WL, Han S, Rui X, Chen XH, Jiang M, Zhang QQ, Wu JJ, Li W (2017) Structural characterization and antioxidant property of released exopolysaccharides from Lactobacillus delbrueckii ssp. bulgaricus SRFM-1. Carbohydr Polym 173:654–664. https://doi.org/10.1016/j.carbpol.2017.06.039
Townsley L, Yannarell SM, Huynh TN, Woodward JJ, Shank EA (2018) Cyclic di-AMP acts as an extracellular signal that impacts Bacillus subtilis biofilm formation and plant attachment. mBio 9(2):e00341–e00318. https://doi.org/10.1128/mBio.00341-18
Turner MS, Xiang Y, Liang ZX, Marcellin E, Pham HT (2023) Cyclic-di-AMP signalling in lactic acid bacteria. FEMS Microbiol Rev 47(3):fuad025. https://doi.org/10.1093/femsre/fuad025
Urshev ZL, Dimitrov ZP, Fatchikova NS, Petrova IG, Ishlimova DI (2008) Partial characterization and dynamics of synthesis of high molecular mass exopolysaccharides from Lactobacillus delbrueckii ssp. bulgaricus and Streptococcus thermophilus. World J Microb Biot 24(2):171–179. https://doi.org/10.1007/s11274-007-9453-0
Vallejo-García LC, Sánchez-Olmos MDC, Gutiérrez-Ríos RM, López Munguía A (2023) Glycosyltransferases expression changes in Leuconostoc mesenteroides subsp. mesenteroides ATCC 8293 grown on different carbon sources. Foods 12(9):1893. https://doi.org/10.3390/foods12091893
Van Calsteren MR, Gagnon F, Nishimura J, Makino S (2015) Structure determination of the neutral exopolysaccharide produced by Lactobacillus delbrueckii subsp. bulgaricus OLL1073R-1. Carbohydr Res 413:115–122. https://doi.org/10.1016/j.carres.2015.05.015
van Kranenburg R, Marugg JD, Swam IIV, Willem NJ, Devos WM (1997) Molecular characterization of the plasmid encoded eps gene cluster essential for exopolysaccharide biosynthesis in Lactococcus lactis. Mol Microbiol 24:387–397. https://doi.org/10.1046/j.1365-2958.1997
van Kranenburg R, Vos HR, van Swam II, Kleerebezem M, de Vos WM (1999) Functional analysis of glycosyltransferase genes from Lactococcus lactis and other gram-positive cocci: complementation, expression, and diversity. J Bacteriol 181(20):6347–6353. https://doi.org/10.1128/JB.181.20.6347-6353.1999
Vastano V, Perrone F, Marasco R, Sacco M, Muscariello L (2016) Transcriptional analysis of exopolysaccharides biosynthesis gene clusters in Lactobacillus plantarum. Arch Microbiol 198(3):295–300. https://doi.org/10.1007/s00203-015-1169-1
Wang C, Cui Y, Qu X (2018) Identification of proteins regulated by acid adaptation related two component system HPK1/RR1 in Lactobacillus delbrueckii subsp. bulgaricus. Arch Microbiol 200(9):1381–1393. https://doi.org/10.1007/s00203-018-1552-9
Warner JB, Lolkema JS (2003) CcpA-dependent carbon catabolite repression in bacteria. Microbiol Mol Biol Rev 67(4):475–490. https://doi.org/10.1128/MMBR.67.4.475-490.2003
Whiteley M, Diggle SP, Greenberg EP (2017) Progress in and promise of bacterial quorum sensing research. Nature 551(7680):313–320. https://doi.org/10.1038/nature24624
Whitney JC, Howell PL (2013) Synthase-dependent exopolysaccharide secretion in Gram-negative bacteria. Trends Microbiol 21:63–72. https://doi.org/10.1016/j.tim.2012.10.001
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. https://doi.org/10.3389/fmicb.2018.00445
Wu J, Han X, Ye M, Li Y, Wang X, Zhong Q (2022) Exopolysaccharides synthesized by lactic acid bacteria: biosynthesis pathway, structure-function relationship, structural modification and applicability. Crit Rev Food Sci Nutr 1–22. https://doi.org/10.1080/10408398.2022.2043822
Xia W, Han J, Zhu S, Wang Y, Zhang W, Wu Z (2023) Structural elucidation of the exopolysaccharide from Streptococcus thermophilus XJ53 and the effect of its molecular weight on immune activity. Int J Biol Macromol 230:123177. https://doi.org/10.1016/j.ijbiomac.2023.123177
Xiao L, Yang Y, Han S, Rui X, Ma K, Zhang C, Wang G, Li W (2023) Effects of genes required for exopolysaccharides biosynthesis in Lacticaseibacillus paracasei S-NB on cell surface characteristics and probiotic properties. Int J Biol Macromol 224:292–305. https://doi.org/10.1016/j.ijbiomac.2022.10.124
Yan N (2013) Structural advances for the major facilitator superfamily (MFS) transporters. Trends Biochem Sci 38(3):151–159. https://doi.org/10.1016/j.tibs.2013.01.003
Yang Y, Jiang G, Tian Y (2023) Biological activities and applications of exopolysaccharides produced by lactic acid bacteria: a mini-review. World J Microbiol Biotechnol 39(6):155. https://doi.org/10.1007/s11274-023-03610-7
Ye G, Chen Y, Wang C, Yang R, Bin X (2018) Purification and characterization of exopolysaccharide produced by Weissella cibaria YB-1 from pickle chinese cabbage. Int J Biol Macromol 120(Pt A):1315–1321. https://doi.org/10.1016/j.ijbiomac.2018.09.019
Zannini E, Waters DM, Coffey A, Arendt EK (2016) Production, properties, and industrial food application of lactic acid bacteria-derived exopolysaccharides. Appl Microbiol Biotechnol 100(3):1121–1135. https://doi.org/10.1007/s00253-015-7172-2
Zhai Z, Xie S, Zhang H, Yi H, Hao Y (2021) Homologous over-expression of chain length determination protein EpsC increases the molecular weight of exopolysaccharide in Streptococcus thermophilus 05–34. Front Microbiol 12:696222. https://doi.org/10.3389/fmicb.2021.696222
Zhang G, Liu L, Li C (2020) Effects of ccpA gene deficiency in Lactobacillus delbrueckii subsp. bulgaricus under aerobic conditions as assessed by proteomic analysis. Microb Cell Fact 19(1):9. https://doi.org/10.1186/s12934-020-1278-7
Zhao D, Jiang J, Du R, Guo S, Ping W, Ling H, Ge J (2019) Purification and characterization of an exopolysaccharide from Leuconostoc lactis L2. Int J Biol Macromol 139:1224–1231. https://doi.org/10.1016/j.ijbiomac.2019.08.114
Zhao X, Liang Q, Song X, Zhang Y (2023) Whole genome sequence of lactiplantibacillus plantarum MC5 and comparative analysis of eps gene clusters. Front Microbiol 14:1146566. https://doi.org/10.3389/fmicb.2023.1146566
Zheng J, Wittouck S, Salvetti E, Franz CMAP, Harris HMB, Mattarelli P, O’Toole PW, Pot B, Vandamme P, Walter J, Watanabe K, Wuyts S, Felis GE, Gänzle MG, Lebeer S (2020) A taxonomic note on the genus Lactobacillus: description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int J Syst Evol Microbiol 70(4):2782–2858. https://doi.org/10.1099/ijsem.0.004107
Zhou Y, Cui Y, Qu X (2019) Exopolysaccharides of lactic acid bacteria: structure, bioactivity and associations: a review. Carbohydr Polym 207:317–332. https://doi.org/10.1016/j.carbpol.2018.11.093
Zhou Y, Cui Y, Suo C, Wang Q, Qu X (2021) Structure, physicochemical characterization, and antioxidant activity of the highly arabinose-branched exopolysaccharide EPS-M2 from Streptococcus thermophilus CS6. Int J Biol Macromol 192:716–727. https://doi.org/10.1016/j.ijbiomac.2021.10.047
Zhou Y, Cui Y, Qu X (2022) Comparative transcriptome analysis for the biosynthesis of antioxidant exopolysaccharide in Streptococcus thermophilus CS6. J Sci Food Agric 102(12):5321–5332. https://doi.org/10.1002/jsfa.11886
Zhu Y, Pham TH, Nhiep TH, Vu NM, Marcellin E, Chakrabortti A, Wang Y, Waanders J, Lo R, Huston WM, Bansal N, Nielsen LK, Liang ZX, Turner MS (2016) Cyclic-di-AMP synthesis by the diadenylate cyclase CdaA is modulated by the peptidoglycan biosynthesis enzyme GlmM in Lactococcus lactis. Mol Microbiol 99(6):1015–1027. https://doi.org/10.1111/mmi.13281
Zikmanis P, Brants K, Kolesovs S, Semjonovs P (2020) Extracellular polysaccharides produced by bacteria of the Leuconostoc genus. World J Microbiol Biotechnol 36(11):161. https://doi.org/10.1007/s11274-020-02937-9
Zotta T, Ricciardi A, Guidone A, Sacco M, Muscariello L, Mazzeo MF, Cacace G, Parente E (2012) Inactivation of ccpA and aeration affect growth, metabolite production and stress tolerance in Lactobacillus plantarum WCFS1. Int J Food Microbiol 155(1–2):51–59. https://doi.org/10.1016/j.ijfoodmicro.2012.01.017
Author information
Authors and Affiliations
Contributions
Yanhua Cui and Shiyuan Dong wrote the main manuscript. Xiaojun Qu prepared Figs. 1, 2 and 3. All authors reviewed the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Conflict of interest
All authors declare that they have no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Cui, Y., Dong, S. & Qu, X. New progress in the identifying regulatory factors of exopolysaccharide synthesis in lactic acid bacteria. World J Microbiol Biotechnol 39, 301 (2023). https://doi.org/10.1007/s11274-023-03756-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11274-023-03756-4