Skip to main content
SpringerLink
Log in

Synbiotics: a New Route of Self-production and Applications to Human and Animal Health

  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

Synbiotics are preparations in which prebiotics are added to probiotics to achieve superior performance and benefits on the host. A new route of their formation is to induce the prebiotic biosynthesis within the probiotic for synbiotic self-production or autologous synbiotics. The aim of this review paper is first to overview the basic concept and (updated) definitions of synergistic synbiotics, and then to focus particularly on the prebiotic properties of probiotic wall components while describing the environmental factors/stresses that stimulate autologous synbiotics, that is, the biosynthesis of prebiotic-forming microcapsule by probiotic bacteria, and finally to present some of their applications to human and animal health.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Swanson KS, Gibson GR, Hutkins R et al (2020) The international scientific association for probiotics and prebiotics (ISAPP) consensus statement on the definition and scope of synbiotics. Nat Rev Gastroenterol Hepatol 17:687–701. https://doi.org/10.1038/s41575-020-0344-2

    Article  PubMed  PubMed Central  Google Scholar 

  2. Fazelnia K, Fakhraei J, Yarahmadi HM, Amini K (2021) Dietary supplementation of potential probiotics Bacillus subtilis, Bacillus licheniformis, and Saccharomyces cerevisiae and synbiotic improves growth performance and immune responses by modulation in intestinal system in broiler chicks challenged with Salmonella Typhimurium. Probiotics Antimicrob Proteins 13:1081–1092. https://doi.org/10.1007/s12602-020-09737-5

    Article  CAS  PubMed  Google Scholar 

  3. Malik JK, Ahmad AH, Kalpana S, Prakash A, Gupta RC (2016) Synbiotics: safety and toxicity considerations. In: Gupta RC (ed) Nutraceuticals, 1st edn. Academic Press, Boston, pp 811–822

    Chapter  Google Scholar 

  4. Helal M, Hussein M-D, Osman M, Shalaby AS, Ghaly M (2015) Production and prebiotic activity of exopolysaccharides derived from some probiotics. Egypt Pharm J 14:1–9. https://doi.org/10.4103/1687-4315.154687

    Article  Google Scholar 

  5. Gibson GR, Hutkins R, Sanders ME et al (2017) Expert consensus document: the international scientific association for probiotics and prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol 14:491–502. https://doi.org/10.1038/nrgastro.2017.75

    Article  PubMed  Google Scholar 

  6. Lordan C, Thapa D, Ross R, Cotter P (2019) Potential for enriching next-generation health-promoting gut bacteria through prebiotics and other dietary components. Gut Microbes 11:1–20. https://doi.org/10.1080/19490976.2019.1613124

    Article  PubMed  PubMed Central  Google Scholar 

  7. Terpou A, Papadaki A, Lappa I, Kachrimanidou V, Bosnea L, Kopsahelis N (2019) Probiotics in food systems: significance and emerging strategies towards improved viability and delivery of enhanced beneficial value. Nutrients 11. https://doi.org/10.3390/nu11071591

  8. Roobab U, Batool Z, Manzoor MF, Shabbir MA, Khan MR, Aadil RM (2020) Sources, formulations, advanced delivery and health benefits of probiotics. Curr Opin Food Sci 32:17–28. https://doi.org/10.1016/j.cofs.2020.01.003

    Article  Google Scholar 

  9. Silva DR, Sardi JdCO, Pitangui NdS, Roque SM, Silva ACBd, Rosalen PL (2020) Probiotics as an alternative antimicrobial therapy: current reality and future directions. J Funct Foods 73:104080. https://doi.org/10.1016/j.jff.2020.104080

  10. 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. https://doi.org/10.3389/fmicb.2019.00841

    Article  PubMed  PubMed Central  Google Scholar 

  11. Shori AB (2017) Microencapsulation improved probiotics survival during gastric transit. HAYATI J Biosci 24:1–5. https://doi.org/10.1016/j.hjb.2016.12.008

    Article  Google Scholar 

  12. Rovinaru C, Pasarin D (2020) Application of microencapsulated synbiotics in fruit-based beverages. Probiotics Antimicrob Proteins 12:764–773. https://doi.org/10.1007/s12602-019-09579-w

    Article  PubMed  Google Scholar 

  13. Cui L-H, Yan C-R, Li H-S et al (2018) A new method of producing a natural antibacterial peptide by encapsulated probiotics internalized with inulin nanoparticles as prebiotics. J Microbiol Biotechnol 28:510–519. https://doi.org/10.4014/jmb.1712.12008

    Article  CAS  PubMed  Google Scholar 

  14. Garcia-Diaz M, Birch D, Wan F, Nielsen H (2017) The role of mucus as an invisible cloak to transepithelial drug delivery by nanoparticles. Adv Drug Deliv Rev 124:107–124. https://doi.org/10.1016/j.addr.2017.11.002

    Article  CAS  PubMed  Google Scholar 

  15. Milea ȘA, Vasile MA, Crăciunescu O et al (2020) Co-microencapsulation of flavonoids from yellow onion skins and lactic acid bacteria lead to multifunctional ingredient for nutraceutical and pharmaceutics applications. Pharmaceutics 12:1053. https://doi.org/10.3390/pharmaceutics12111053

    Article  CAS  PubMed Central  Google Scholar 

  16. Ephrem E, Najjar A, Charcosset C, Greige-Gerges H (2018) Encapsulation of natural active compounds, enzymes, and probiotics for fruit juice fortification, preservation, and processing: an overview. J Funct Foods 48:65–84. https://doi.org/10.1016/j.jff.2018.06.021

    Article  CAS  Google Scholar 

  17. Yus Argón C, Gracia R, Larrea A et al (2019) Targeted release of probiotics from enteric microparticulated formulations. Polymers 11:1668. https://doi.org/10.3390/polym11101668

    Article  CAS  Google Scholar 

  18. Papadimitriou K, Alegría Á, Bron PA et al (2016) Stress physiology of lactic acid bacteria. Microbiol Mol Biol Rev 80:837–890. https://doi.org/10.1128/MMBR.00076-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Nguyen HT, Razafindralambo H, Blecker C, N’Yapo C, Thonart P, Delvigne F (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. https://doi.org/10.1016/j.bej.2014.04.005

    Article  CAS  Google Scholar 

  20. Nguyen P-T, Nguyen T-T, Vo T-N-T, Nguyen T-T-X, Hoang Q-K, Nguyen H-T (2021) Response of Lactobacillus plantarum VAL6 to challenges of pH and sodium chloride stresses. Sci Rep 11:1301. https://doi.org/10.1038/s41598-020-80634-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Kim SK, Guevarra RB, Kim YT et al (2019) Role of probiotics in human gut microbiome-associated diseases. J Microbiol Biotechnol 29:1335–1340. https://doi.org/10.4014/jmb.1906.06064

    Article  PubMed  Google Scholar 

  22. Markowiak P, Śliżewska K (2018) The role of probiotics, prebiotics and synbiotics in animal nutrition. Gut Pathogens 10:21. https://doi.org/10.1186/s13099-018-0250-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Davani-Davari D, Negahdaripour M, Karimzadeh I et al (2019) Prebiotics: Definition, types, sources, mechanisms, and clinical applications. Foods 8:92. https://doi.org/10.3390/foods8030092

    Article  CAS  PubMed Central  Google Scholar 

  24. Grosu-Tudor S, Zamfir M, Meulen R, Falony G, Vuyst LC (2013) Prebiotic potential of some exopolysaccharides produced by lactic acid bacteria. Romanian Biotechnol Lett 18:8666–8676. https://www.rombio.eu/vol18nr5/13%20Grosu-Tudor%20and%20Zamfir.pdf. Accessed 22 Apr 2022

  25. Quero CD, Manonelles P, Fernández M, Abellán-Aynés O, López-Plaza D, Andreu-Caravaca L, Hinchado MD, Gálvez I, Ortega E (2021) Differential health effects on inflammatory, immunological and stress parameters in professional soccer players and sedentary individuals after consuming a synbiotic. A triple-blinded, randomized, placebo-controlled pilot study. Nutrients 13. https://doi.org/10.3390/nu13041321

  26. Swanson KS, Collado MC, Endo A et al (2020) The international scientific association for probiotics and prebiotics (ISAPP) consensus statement on the definition and scope of synbiotics. Nat Rev Gastroenterol Hepatol 17:687–701. https://doi.org/10.1038/s41575-020-0344-2

    Article  PubMed  PubMed Central  Google Scholar 

  27. Kolida S, Gibson G (2011) Synbiotics in health and disease. Ann Rev Food Sci Technol 2:373–393. https://doi.org/10.1146/annurev-food-022510-133739

    Article  Google Scholar 

  28. Krausova G, Hynstova I, Svejstil R, Mrvikova I, Kadlec R (2021) Identification of synbiotics conducive to probiotics adherence to intestinal mucosa using an in vitro Caco-2 and HT29-MTX cell model. Processes 9. https://doi.org/10.3390/pr9040569

  29. Celebioglu HU, Olesen SV, Prehn K et al (2017) Mucin- and carbohydrate-stimulated adhesion and subproteome changes of the probiotic bacterium Lactobacillus acidophilus NCFM. J Proteom 163:102–110. https://doi.org/10.1016/j.jprot.2017.05.015

    Article  CAS  Google Scholar 

  30. Wang Y, Jiang Y, Deng Y et al (2020) Probiotic supplements: hope or hype? Front Microbiol 11:160. https://doi.org/10.3389/fmicb.2020.00160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Nunpan S, Suwannachart C, Wayakanon K (2019) Effect of prebiotics-enhanced probiotics on the growth of Streptococcus mutans. Int J Microbiol 2019:4623807. https://doi.org/10.1155/2019/4623807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. MAA S (2014) Dysbiosis, probiotics, synbiotics and human health. Austin J Nutr Food Sci 2:1044. https://austinpublishinggroup.com/nutrition-food-sciences/fulltext/ajnfs-v2-id1044.php. Accessed 22 Apr 2022

  33. de Vrese M, Schrezenmeir J (2008) Probiotics, prebiotics, and synbiotics. Springer, Berlin

    Google Scholar 

  34. Krumbeck J, Walter J, Hutkins R (2018) Synbiotics for improved human health: recent developments, challenges, and opportunities. Ann Rev Food Sci Technol 9:451–479. https://doi.org/10.1146/annurev-food-030117-012757

    Article  Google Scholar 

  35. Pandey K, Naik S, Vakil B (2015) Probiotics, prebiotics and synbiotics- a review. J Food Sci Technol 52:7577–7587. https://doi.org/10.1007/s13197-015-1921-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Chapot-Chartier M-P, Kulakauskas S (2014) Cell wall structure and function in Lactic acid bacteria. Microb Cell Fact 13:S9. https://doi.org/10.1186/1475-2859-13-S1-S9

    Article  PubMed  PubMed Central  Google Scholar 

  37. Lebeer S, Vanderleyden J, Keersmaecker S (2010) Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat Rev Microbiol 8:171–184. https://doi.org/10.1038/nrmicro2297

    Article  CAS  PubMed  Google Scholar 

  38. Kleerebezem M, Hols B, Bernard E et al (2010) The extracellular biology of the Lactobacilli. FEMS Microbiol Rev 34:199–230. https://doi.org/10.1111/j.1574-6976.2010.00208.x

    Article  CAS  PubMed  Google Scholar 

  39. Lebeer S, Vanderleyden J, De Keersmaecker SCJ (2008) Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev 72:728. https://doi.org/10.1128/MMBR.00017-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Delcour J, Ferain T, Deghorain M, Palumbo E, Hols P (1999) The biosynthesis and functionality of the cell-wall of lactic acid bacteria. Antonie Van Leeuwenhoek 76:159–184. https://doi.org/10.1023/A:1002089722581

    Article  CAS  PubMed  Google Scholar 

  41. Neuhaus F, Baddiley J (2004) A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in gram-positive bacteria. Microbiol Mol Biol Rev 67:686–723. https://doi.org/10.1128/MMBR.67.4.686-723.2003

    Article  CAS  Google Scholar 

  42. Claes I, Segers ME, Verhoeven TLA et al (2012) Lipoteichoic acid is an important microbe-associated molecular pattern of Lactobacillus rhamnosus GG. Microb Cell Fact 11:161. https://doi.org/10.1186/1475-2859-11-161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Granato D, Perotti F, Masserey I, Rouvet M, Golliard M, Servin A, Brassart D (1999) Cell surface-associated lipoteichoic acid acts as an adhesion factor for attachment of Lactobacillus johnsonii La1 to human enterocyte-like Caco-2 cells. Appl Environ Microbiol 65:1071–1077. https://doi.org/10.1128/AEM.65.3.1071-1077.1999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Buck B, Altermann E, Svingerud T, Klaenhammer T (2006) Functional analysis of putative adhesion factors in Lactobacillus acidophilus NCFM. Appl Environ Microbiol 71:8344–8351. https://doi.org/10.1128/AEM.71.12.8344-8351.2005

    Article  CAS  Google Scholar 

  45. Smit E, Jager D, Martinez B, Tielen F, Pouwels P (2003) Structural and functional analysis of the S-layer protein crystallisation domain of Lactobacillus acidophilus ATCC 4356: evidence for protein–protein interaction of two subdomains. J Mol Biol 324:953–964. https://doi.org/10.1016/S0022-2836(02)01135-X

    Article  Google Scholar 

  46. Chapot-Chartier MP, Vinogradov E, Sadovskaya I et al (2010) Cell surface of Lactococcus lactis is covered by a protective polysaccharide pellicle. J Biol Chem 285:10464–10471. https://doi.org/10.1074/jbc.M109.082958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Yasuda E, Serata M, Sako T (2008) Suppressive effect on activation of macrophages by Lactobacillus casei strain Shirota genes determining the synthesis of cell wall-associated polysaccharides. Appl Environ Microbiol 74:4746–4755. https://doi.org/10.1128/AEM.00412-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Lebeer S, Claes I, Verhoeven T, Vanderleyden J, Keersmaecker S (2010) Exopolysaccharides of Lactobacillus rhamnosus GG form a protective shield against innate immune factors in the intestine. Microb Biotechnol 4:368–374. https://doi.org/10.1111/j.1751-7915.2010.00199.x

    Article  CAS  PubMed  Google Scholar 

  49. 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. https://doi.org/10.1111/1541-4337.12554

    Article  PubMed  Google Scholar 

  50. Grujović M, Mladenović K, Nikodijević D, Čomić L (2019) Autochthonous lactic acid bacteria-presentation of potential probiotics application. Biotechnol Lett 41:1319–1331. https://doi.org/10.1007/s10529-019-02729-8

    Article  CAS  PubMed  Google Scholar 

  51. Bove P, Russo P, Capozzi V, Gallone A, Spano G, Fiocco D (2013) Lactobacillus plantarum passage through an oro-gastro-intestinal tract simulator: carrier matrix effect and transcriptional analysis of genes associated to stress and probiosis. Microbiol Res 168:351–359. https://doi.org/10.1016/j.micres.2013.01.004

    Article  CAS  PubMed  Google Scholar 

  52. Ferrando V, Quiberoni A, Reinheimer J, Suárez V (2016) Functional properties of Lactobacillus plantarum strains: a study in vitro of heat stress influence. Food Microbiol 54:154–161. https://doi.org/10.1016/j.fm.2015.10.003

    Article  CAS  Google Scholar 

  53. Chen M-J, Tang H-Y, Chiang M-L (2017) Effects of heat, cold, acid and bile salt adaptations on the stress tolerance and protein expression of kefir-isolated probiotic Lactobacillus kefiranofaciens M1. Food Microbiol 66:20–27. https://doi.org/10.1016/j.fm.2017.03.020

    Article  CAS  PubMed  Google Scholar 

  54. Hernández-Alcántara AM, Wacher C, Llamas MG, López P, Pérez-Chabela ML (2018) Probiotic properties and stress response of thermotolerant lactic acid bacteria isolated from cooked meat products. LWT 91:249–257. https://doi.org/10.1016/j.lwt.2017.12.063

    Article  CAS  Google Scholar 

  55. Haddaji N, Boubaker K, Lagha R, Khouadja S, Bakhrouf A (2015) Effect of high temperature on viability of Lactobacillus casei and analysis of secreted and GroEL proteins profiles. J Bacteriol Res 7:29–34. https://doi.org/10.5897/JBR2015.0155

    Article  Google Scholar 

  56. Varmanen P, Savijoki K (2011) Responses of Lactic Acid Bacteria to heat stress. In: E. Tsakalidou KP (ed) Stress responses of Lactic Acid Bacteria, 1st edn. Springer, New York, pp 55–66

  57. Fonseca F, Girardeau A, Passot S (2021) Freeze-drying of lactic acid bacteria: a stepwise approach for developing a freeze-drying protocol based on physical properties. In: Wolkers WF, Oldenhof H (eds) Cryopreservation and Freeze-Drying Protocols, 1st edn. Springer, US, New York, NY, pp 703–719

    Chapter  Google Scholar 

  58. Song S, Bae D-W, Lim K, Griffiths MW, Oh S (2014) Cold stress improves the ability of Lactobacillus plantarum L67 to survive freezing. Int J Food Microbiol 191:135–143. https://doi.org/10.1016/j.ijfoodmicro.2014.09.017

    Article  PubMed  Google Scholar 

  59. Keto-Timonen R, Hietala N, Palonen E, Hakakorpi A, Lindström M, Korkeala H (2016) Cold shock proteins: a minireview with special emphasis on Csp-family of Enteropathogenic Yersinia. Front Microbiol 7:1151. https://doi.org/10.3389/fmicb.2016.01151

    Article  PubMed  PubMed Central  Google Scholar 

  60. Mangiagalli M, Sarusi G, Kaleda A et al (2018) Structure of a bacterial ice binding protein with two faces of interaction with ice. The FEBS J 285:1653–1666. https://doi.org/10.1111/febs.14434

    Article  CAS  PubMed  Google Scholar 

  61. Polo L, Mañes-Lázaro R, Olmeda I, Cruz-Pio LE, Medina Á, Ferrer S, Pardo I (2017) Influence of freezing temperatures prior to freeze-drying on viability of yeasts and lactic acid bacteria isolated from wine. J Appl Microbiol 122:1603–1614. https://doi.org/10.1111/jam.13465

    Article  CAS  PubMed  Google Scholar 

  62. Haddaji N, Khouadja S, Fdhila K et al (2015) Acid stress suggests different determinants for polystyrene and HeLa cell adhesion in Lactobacillus casei. J Dairy Sci 98:4302–4309. https://doi.org/10.3168/jds.2014-9198

    Article  CAS  PubMed  Google Scholar 

  63. Mills S, Stanton C, Fitzgerald G, Ross R (2011) Enhancing the stress responses of probiotics for a lifestyle from gut to product and back again. Microb Cell Fact 10(Suppl 1):S19. https://doi.org/10.1186/1475-2859-10-S1-S19

    Article  PubMed  PubMed Central  Google Scholar 

  64. Sánchez B, Champomier-Vergès M-C, Collado MdC et al (2007) Low-pH adaptation and the acid tolerance response of Bifidobacterium longum biotype longum. Appl Environ Microbiol 73:6450–6459. https://doi.org/10.1128/AEM.00886-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Wang C, Cui Y, Qu X (2018) Mechanisms and improvement of acid resistance in lactic acid bacteria. Arch Microbiol 200:195–201. https://doi.org/10.1007/s00203-017-1446-2

    Article  CAS  PubMed  Google Scholar 

  66. Pérez B, Benomar N, Gómez NC et al (2017) Proteomic analysis of Lactobacillus pentosus for the identification of potential markers involved in acid resistance and their influence on other probiotic features. Food Microbiol 72:31–38. https://doi.org/10.1016/j.fm.2017.11.006

    Article  CAS  Google Scholar 

  67. Pato U, Surono IS (2013) Bile and acid tolerance of lactic acid bacteria isolated from tempoyak and their probiotic potential. Int J Agric Technol 9:1849–1862. https://www.thaiscience.info/journals/Article/IJAT/10895726.pdf. Accessed 22 Apr 2022

  68. Endo A, Dicks LMT (2014) Physiology of the LAB. In Holzapfel WH, Wood BJ (eds) Lactic Acid Bacteria, 1st edn. Wiley, New York, pp 13–30. https://doi.org/10.1002/9781118655252.ch2

  69. Zhang W, Guo H, Cao C et al (2017) Adaptation of Lactobacillus casei Zhang to gentamycin involves an alkaline shock protein. Front Microbiol 8:2316. https://doi.org/10.3389/fmicb.2017.02316

    Article  PubMed  PubMed Central  Google Scholar 

  70. Cao M, Kobel PA, Morshedi MM, Wu MFW, Paddon C, Helmann JD (2002) Defining the Bacillus subtilis σW regulon: a comparative analysis of promoter consensus search, run-off transcription/macroarray analysis (ROMA), and transcriptional profiling approaches. J Mol Biol 316:443–457. https://doi.org/10.1006/jmbi.2001.5372

    Article  CAS  PubMed  Google Scholar 

  71. Palomino MM, Waehner PM, Martin JF et al (2016) Influence of osmotic stress on the profile and gene expression of surface layer proteins in Lactobacillus acidophilus ATCC 4356. Appl Microbiol Biotechnol 100:8475–8484. https://doi.org/10.1007/s00253-016-7698-y

    Article  CAS  PubMed  Google Scholar 

  72. Yin X, Weitzel F, Jiménez-López C et al (2020) Directing Effect of bacterial extracellular polymeric substances (EPS) on calcite organization and EPS–carbonate composite aggregate formation. Crystal Growth Design 20:1467–1484. https://doi.org/10.1021/acs.cgd.9b01113

    Article  CAS  Google Scholar 

  73. Mack D, Michail S, Wei S, McDougall L, Hollingsworth M (1999) Probiotics inhibit enteropathogenic E. Coli adherence in vitro by inducing intestinal mucin gene expression. American J Physiol 276:G941-950. https://doi.org/10.1152/ajpgi.1999.276.4.G941

    Article  CAS  Google Scholar 

  74. Fonseca HC, de Sousa MD, Ramos CL, Dias DR, Schwan RF (2021) Probiotic properties of lactobacilli and their ability to inhibit the adhesion of Enteropathogenic bacteria to Caco-2 and HT-29 cells. Probiotics Antimicrob Proteins 13:102–112. https://doi.org/10.1007/s12602-020-09659-2

    Article  CAS  PubMed  Google Scholar 

  75. Maldonado Galdeano C, Cazorla SI, Lemme Dumit JM, Vélez E, Perdigón G (2019) Beneficial effects of probiotic consumption on the immune system. Ann Nutr Metabol 74:115–124. https://doi.org/10.1159/000496426

    Article  CAS  Google Scholar 

  76. Gerbino E, Carasi P, Mobili P, Serradell MA, Gómez-Zavaglia A (2015) Role of S-layer proteins in bacteria. World J Microbiol Biotechnol 31:1877–1887. https://doi.org/10.1007/s11274-015-1952-9

    Article  CAS  PubMed  Google Scholar 

  77. Hynönen U, Kant R, Lähteinen T et al (2014) Functional characterization of probiotic surface layer protein-carrying Lactobacillus amylovorus strains. BMC Microbiol 14:199. https://doi.org/10.1186/1471-2180-14-199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Scholz H, Riedmann E, Witte A, Lubitz W, Kuen B (2001) S-Layer variation in Bacillus stearothermophilus PV72 is based on dna rearrangements between the chromosome and the naturally occurring megaplasmids. J Bacteriol 183:1672–1679. https://doi.org/10.1128/JB.183.5.1672-1679.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Jakava-Viljanen M, Avall-Jääskeläinen S, Messner P, Sleytr UB, Palva A (2002) Isolation of three new surface layer protein genes (slp) from Lactobacillus brevis ATCC 14869 and characterization of the change in their expression under aerated and anaerobic conditions. J Bacteriol 184:6786–6795. https://doi.org/10.1128/JB.184.24.6786-6795.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Schär-Zammaretti P, Dillmann M-L, D’Amico N, Affolter M, Ubbink J (2006) Influence of fermentation medium composition on physicochemical surface properties of Lactobacillus acidophilus. Appl Environ Microbiol 71:8165–8173. https://doi.org/10.1128/AEM.71.12.8165-8173.2005

    Article  CAS  Google Scholar 

  81. Marco ML, Vries MCd, Wels M et al (2010) Convergence in probiotic Lactobacillus gut-adaptive responses in humans and mice. The ISME J 4:1481–1484. https://doi.org/10.1038/ismej.2010.61

    Article  CAS  PubMed  Google Scholar 

  82. Grosu-Tudor S-S, Brown L, Hebert EM et al (2016) S-layer production by Lactobacillus acidophilus IBB 801 under environmental stress conditions. Appl Microbiol Biotechnol 100:4573–4583. https://doi.org/10.1007/s00253-016-7355-5

    Article  CAS  PubMed  Google Scholar 

  83. Sukhithasri V, Nisha N, Biswas L, Kumar VA, Biswas R (2013) Innate immune recognition of microbial cell wall components and microbial strategies to evade such recognitions. Microbiol Res 168:396–406. https://doi.org/10.1016/j.micres.2013.02.005

    Article  CAS  Google Scholar 

  84. Huang J, Li J, Li Q et al (2020) Peptidoglycan derived from Lactobacillus rhamnosus MLGA up-regulates the expression of chicken beta-defensin 9 without triggering an inflammatory response. Innate Immun 26:733–745. https://doi.org/10.1177/1753425920949917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Wu C, Zhang J, Chen W, Wang M, Du G, Chen J (2012) A combined physiological and proteomic approach to reveal lactic-acid-induced alterations in Lactobacillus casei Zhang and its mutant with enhanced lactic acid tolerance. Appl Microbiol Biotechnol 93:707–722. https://doi.org/10.1007/s00253-011-3757-6

    Article  CAS  PubMed  Google Scholar 

  86. 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. https://doi.org/10.1371/journal.pone.0050777

  87. Jin J, Qin Q, Guo H et al (2015) Effect of pre-stressing on the acid-stress response in Bifidobacterium revealed using proteomic and physiological approaches. PLoS ONE 10:e0117702. https://doi.org/10.1371/journal.pone.0117702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Ramos AN, Sesto Cabral ME, Noseda D, Bosch A, Yantorno OM, Valdez JC (2012) Antipathogenic properties of Lactobacillus plantarum on Pseudomonas aeruginosa: the potential use of its supernatants in the treatment of infected chronic wounds. Wound Repair Regen 20:552–562. https://doi.org/10.1111/j.1524-475X.2012.00798.x

    Article  PubMed  Google Scholar 

  89. İspirli H, Demirbaş F, Dertli E (2018) Glucan type exopolysaccharide (EPS) shows prebiotic effect and reduces syneresis in chocolate pudding. J Food Sci Technol 55:3821–3826. https://doi.org/10.1007/s13197-018-3181-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Hongpattarakere T, Cherntong N, Wichienchot S, Kolida S, Rastall RA (2012) In vitro prebiotic evaluation of exopolysaccharides produced by marine isolated lactic acid bacteria. Carbohydr Polym 87:846–852. https://doi.org/10.1016/j.carbpol.2011.08.085

    Article  CAS  PubMed  Google Scholar 

  91. Collado MC, Gueimonde M, Sanz Y, Salminen S (2006) Adhesion properties and competitive pathogen exclusion ability of Bifidobacteria with acquired acid resistance. J Food Prot 69:1675–1679. https://doi.org/10.4315/0362-028X-69.7.1675

    Article  PubMed  Google Scholar 

  92. Nguyen P-T, Nguyen T-T, Bui D-C et al (2020) Exopolysaccharide production by lactic acid bacteria: the manipulation of environmental stresses for industrial applications. AIMS Microbiol 6:451–469. https://doi.org/10.3934/microbiol.2020027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. 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. https://doi.org/10.1016/S0958-6946(01)00160-1

    Article  CAS  Google Scholar 

  94. Huu Thanh N, Razafindralambo H, Blecker C, Yapo NC, Thonart P, Delvigne F (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. https://doi.org/10.1016/j.bej.2014.04.005

    Article  CAS  Google Scholar 

  95. Gyawali R, Nwamaioha N, Fiagbor R, Zimmerman T, Newman RH, Ibrahim SA (2019) The role of prebiotics in disease prevention and health promotion. In: Watson RR, Preedy VR (eds) Dietary interventions in gastrointestinal diseases, 1st edn. Academic Press, pp 151–167

    Chapter  Google Scholar 

  96. Spinler J, Auchtung J, Brown A et al (2017) Next-generation probiotics targeting Clostridium difficile through precursor-directed antimicrobial biosynthesis. Infect Immun 85:IAI.00303–00317. https://doi.org/10.1128/IAI.00303-17

  97. Newman AM, Arshad M (2020) The Role of Probiotics, Prebiotics and Synbiotics in Combating Multidrug-Resistant Organisms. Clin Ther 42:1637–1648. https://doi.org/10.1016/j.clinthera.2020.06.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Li C, Niu Z, Zou M et al (2020) Probiotics, prebiotics, and synbiotics regulate the intestinal microbiota differentially and restore the relative abundance of specific gut microorganisms. J Dairy Sci 103:5816–5829. https://doi.org/10.3168/jds.2019-18003

    Article  CAS  PubMed  Google Scholar 

  99. Bakhtiary M, Morvaridzadeh M, Agah S et al (2021) Effect of probiotic, prebiotic, and synbiotic supplementation on cardiometabolic and oxidative stress parameters in patients with chronic kidney disease: a systematic review and meta-analysis. Clin Ther 43:e71–e96. https://doi.org/10.1016/j.clinthera.2020.12.021

    Article  CAS  PubMed  Google Scholar 

  100. Scorletti E, Afolabi PR, Miles EA et al (2020) Synbiotics alter fecal microbiomes, but not liver fat or fibrosis, in a randomized trial of patients with nonalcoholic fatty liver disease. Gastroenterology 158:1597-1610.e1597. https://doi.org/10.1053/j.gastro.2020.01.031

    Article  CAS  PubMed  Google Scholar 

  101. Askari G, Ghavami A, Shahdadian F, Moravejolahkami AR (2021) Effect of synbiotics and probiotics supplementation on autoimmune diseases: a systematic review and meta-analysis of clinical trials. Clin Nutr 40:3221–3234. https://doi.org/10.1016/j.clnu.2021.02.015

    Article  CAS  PubMed  Google Scholar 

  102. Mbusa Kambale R, Nancy F, Ngaboyeka G, Kasengi J, Bindels L, Van der Linden D (2020) Effects of probiotics and synbiotics on diarrhea in undernourished children: systematic review with meta-analysis. Clin Nutr 40:3158–3169. https://doi.org/10.1016/j.clnu.2020.12.026

    Article  Google Scholar 

  103. Núñez-Sánchez MA, Herisson FM, Cluzel GL, Caplice NM (2021) Metabolic syndrome and synbiotic targeting of the gut microbiome. Curr Opin Food Sci 41:60–69. https://doi.org/10.1016/j.cofs.2021.02.014

    Article  CAS  Google Scholar 

  104. Malik JK, Prakash A, Srivastava AK, Gupta RC (2019) Synbiotics in animal health and production. In: Gupta R, Srivastava A, Lall R (eds) Nutraceuticals in Veterinary Medicine, 1st edn. Springer, Cham, pp 287–301. https://doi.org/10.1007/978-3-030-04624-8_20

  105. Aftabgard M, Salarzadeh A, Mohseni M (2019) The Effects of a synbiotic mixture of Galacto-oligosaccharides and Bacillus strains in Caspian Salmon, Salmo trutta caspius fingerlings. Probiotics Antimicrob Proteins 11:1300–1308. https://doi.org/10.1007/s12602-018-9498-4

    Article  CAS  PubMed  Google Scholar 

  106. Eslamparast T, Poustchi H, Zamani F, Sharafkhah M, Malekzadeh R, Hekmatdoost A (2014) Synbiotic supplementation in nonalcoholic fatty liver disease: a randomized, double-blind, placebo-controlled pilot study. Am J Clin Nutr 99:535–542. https://doi.org/10.3945/ajcn.113.068890

    Article  CAS  PubMed  Google Scholar 

  107. Neyrinck A, Rodriguez J, Taminiau B et al (2021) Improvement of gastrointestinal discomfort and inflammatory status by a synbiotic in middle-aged adults: a double-blind randomized placebo-controlled trial. Sci Rep 11:2627. https://doi.org/10.1038/s41598-020-80947-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Phavichitr N, Wang S, Chomto S et al (2021) Impact of synbiotics on gut microbiota during early life: a randomized, double-blind study. Sci Rep 11:3534. https://doi.org/10.1038/s41598-021-83009-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Alizadeh M, Munyaka P, Yitbarek A, Echeverry H, Rodriguez-Lecompte JC (2017) Maternal antibody decay and antibody-mediated immune responses in chicken pullets fed prebiotics and synbiotics. Poul Sci 96:58–64. https://doi.org/10.3382/ps/pew244

    Article  CAS  Google Scholar 

  110. Baffoni L, Gaggìa F, Garofolo G et al (2017) Evidence of Campylobacter jejuni reduction in broilers with early synbiotic administration. Int J Food Microbiol 251:41–47. https://doi.org/10.1016/j.ijfoodmicro.2017.04.001

    Article  CAS  PubMed  Google Scholar 

  111. Luoma A, Markazi A, Shanmugasundaram R, Murugesan GR, Mohnl M, Selvaraj R (2017) Effect of synbiotic supplementation on layer production and cecal Salmonella load during a Salmonella challenge. Poul Sci 96:4208–4216. https://doi.org/10.3382/ps/pex251

    Article  CAS  Google Scholar 

  112. Krueger LA, Spangler DA, Vandermyde DR, Sims MD, Ayangbile GA (2017) Avi-Lution® supplemented at 1.0 or 2.0 g/kg in feed improves the growth performance of broiler chickens during challenge with bacitracin-resistant Clostridium perfringens. Poul Sci 96:2595–2600. https://doi.org/10.3382/ps/pex074

    Article  CAS  Google Scholar 

  113. Mohammed A, Mahmoud M, Murugesan R, Cheng HW (2021) Effect of a synbiotic supplement on fear response and memory assessment of broiler chickens subjected to heat stress. Animals 11:427. https://doi.org/10.3390/ani11020427

    Article  PubMed  PubMed Central  Google Scholar 

  114. Bogucka J, Vieira Santos D, Bogusławska-Tryk M, Dankowiakowska A, Da Costa R, Bednarczyk M (2019) Microstructure of the small intestine in broiler chickens fed a diet with probiotic or synbiotic supplementation. J Anim Physiol a Anim Nutr 103:1785–1791. https://doi.org/10.1111/jpn.13182

    Article  CAS  Google Scholar 

  115. Sopková D, Hertelyová Z, Andrejčáková Z et al (2017) The application of probiotics and flaxseed promotes metabolism of n-3 polyunsaturated fatty acids in pigs. J Appl Anim Res 45:93–98. https://doi.org/10.1080/09712119.2015.1124333

    Article  CAS  Google Scholar 

  116. Chae J, Pajarillo EA, Oh JK, Kim H, Kang D-K (2016) Revealing the combined effects of lactulose and probiotic enterococci on the swine faecal microbiota using 454 pyrosequencing. Microb Biotechnol 9:486–495. https://doi.org/10.1111/1751-7915.12370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Czyżewska-Dors E, Kwit K, Stasiak E, Rachubik J, Śliżewska K, Pomorska-Mól M (2018) Effects of newly developed synbiotic and commercial probiotic products on the haematological indices, serum cytokines, acute phase proteins concentration, and serum immunoglobulins amount in sows and growing pigs - A pilot study. J Vet Res 62:317–328. https://doi.org/10.2478/jvetres-2018-0046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Duarte ME, Tyus J, Kim SW (2020) Synbiotic effects of enzyme and probiotics on intestinal health and growth of newly weaned pigs challenged with enterotoxigenic F18+Escherichia coli. Front Vet Sci 7:573. https://doi.org/10.3389/fvets.2020.00573

    Article  PubMed  PubMed Central  Google Scholar 

  119. Lei XJ, Zhang WL, Cheong JY, Lee SI, Kim IH (2018) Effect of antibiotics and synbiotic on growth performance, nutrient digestibility, and faecal microbial shedding in growing-finishing pigs. J Appl Anim Res 46:1202–1206. https://doi.org/10.1080/09712119.2018.1484359

    Article  CAS  Google Scholar 

  120. Marcondes MI, Pereira TR, Chagas JCC et al (2016) Performance and health of Holstein calves fed different levels of milk fortified with symbiotic complex containing pre- and probiotics. Trop Anim Health Prod 48:1555–1560. https://doi.org/10.1007/s11250-016-1127-1

    Article  CAS  PubMed  Google Scholar 

  121. Cavalcante RB, Telli GS, Tachibana L et al (2020) Probiotics, Prebiotics and Synbiotics for Nile tilapia: Growth performance and protection against Aeromonas hydrophila infection. Aquac Rep 17:100343. https://doi.org/10.1016/j.aqrep.2020.100343

    Article  Google Scholar 

  122. Yao W, Li X, Zhang C, Wang J, Cai Y, Leng X (2021) Effects of dietary synbiotics supplementation methods on growth, intestinal health, non-specific immunity and disease resistance of Pacific white shrimp, Litopenaeus vannamei. Fish Shellfish Immunol 112:46–55. https://doi.org/10.1016/j.fsi.2021.02.011

    Article  CAS  PubMed  Google Scholar 

  123. Huynh T-G, Cheng A-C, Chi C-C, Chiu K-H, Liu C-H (2018) A synbiotic improves the immunity of white shrimp, Litopenaeus vannamei: metabolomic analysis reveal compelling evidence. Fish Shellfish Immunol 79:284–293. https://doi.org/10.1016/j.fsi.2018.05.031

    Article  CAS  PubMed  Google Scholar 

  124. Villumsen KR, Ohtani M, Forberg T, Aasum E, Tinsley J, Bojesen AM (2020) Synbiotic feed supplementation significantly improves lipid utilization and shows discrete effects on disease resistance in rainbow trout (Oncorhynchus mykiss). Sci Rep 10:16993. https://doi.org/10.1038/s41598-020-73812-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Hamsah H, Widanarni W, Alimuddin A, Yuhana M, Junior MZ, Hidayatullah D (2019) Immune response and resistance of Pacific white shrimp larvae administered probiotic, prebiotic, and synbiotic through the bio-encapsulation of Artemia sp. Aquac Int 27:567–580. https://doi.org/10.1007/s10499-019-00346-w

    Article  CAS  Google Scholar 

  126. Huynh Truong G, Hu SY, Chiu CS, Truong P, Liu CH (2019) Bacterial population in intestines of white shrimp, Litopenaeus vannamei fed a synbiotic containing Lactobacillus plantarum and galactooligosaccharide. Aquac Res 50. https://doi.org/10.1111/are.13951

  127. Wongsasak U, Chaijamrus S, Kumkhong S, Boonanuntanasarn S (2015) Effects of dietary supplementation with β-glucan and synbiotics on immune gene expression and immune parameters under ammonia stress in Pacific white shrimp. Aquaculture 436:179–187. https://doi.org/10.1016/j.aquaculture.2014.10.028

    Article  CAS  Google Scholar 

  128. Huynh Truong G, Chi C-C, Phuong N, Hien T, Cheng A-C, Liu C-H (2018) Effects of synbiotic containing Lactobacillus plantarum 7–40 and galactooligosaccharide on the growth performance of white shrimp, Litopenaeus vannamei. Aquac Res 49:1–13. https://doi.org/10.1111/are.13701

    Article  CAS  Google Scholar 

  129. Hamid S, Magray S (2012) Impact and manipulation of gut microflora in poultry: a review. J Anim Vet Adv 11:873–877. https://doi.org/10.3923/javaa.2012.873.877

    Article  Google Scholar 

  130. Ashayerizadeh A, Dabiri N, Mirzadeh K, Ghorbani M (2011) Effects of dietary inclusion of several biological feed additives on growth response of broiler chickens. J Cell Anim Biol 5:61–65. https://doi.org/10.5897/JCAB.9000059

    Article  CAS  Google Scholar 

  131. Butt UD, Lin N, Akhter N, Siddiqui T, Li S, Wu B (2021) Overview of the latest developments in the role of probiotics, prebiotics and synbiotics in shrimp aquaculture. Fish Shellfish Immunol 114:263–281. https://doi.org/10.1016/j.fsi.2021.05.003

    Article  CAS  PubMed  Google Scholar 

  132. Fei Y, Chen Z, Han S, Zhang S, Zhang T, Lu Y, Berglund B, Xiao H, Li L, Yao M (2021) Role of prebiotics in enhancing the function of next-generation probiotics in gut microbiota. Crit Rev Food Sci Nutr 29:1–18. https://doi.org/10.1080/10408398.2021.1958744

    Article  CAS  Google Scholar 

  133. Niittynen L, Kajander K, Korpela R (2007) Galacto-oligosaccharides and bowel function. Scand J Food Nutr 51:62–66. https://doi.org/10.1080/17482970701414596

    Article  PubMed Central  Google Scholar 

  134. Rashidinejad A, Bahrami A, Rehman A, Rezaei A, Babazadeh A, Singh H, Jafari SM (2020) Co-encapsulation of probiotics with prebiotics and their application in functional/synbiotic dairy products. Crit Rev Food Sci Nutr 30:1–25. https://doi.org/10.1080/10408398.2020.1854169

    Article  CAS  Google Scholar 

  135. Ma J, Xu C, Liu F, Hou J, Shao H, Yu W (2021) Stress adaptation and cross-protection of Lactobacillus plantarum KLDS 1.0628. CyTA - J Food 19:72–80. https://doi.org/10.1080/19476337.2020.1859619

    Article  CAS  Google Scholar 

Download references

Funding

Phu-Tho Nguyen was funded by Vingroup JSC and supported by the Master, PhD Scholarship Programme of Vingroup Innovation Foundation (VINIF), Institute of Big Data, code VINIF.2021.TS.110.

Author information

Authors and Affiliations

  1. Hutech Institute of Applied Science, HUTECH University, Ho Chi Minh City, Vietnam

    Thi-Tho Nguyen & Minh-Nhut Pham

  2. An Giang University, An Giang, Vietnam

    Phu-Tho Nguyen & Huu-Thanh Nguyen

  3. Vietnam National University, Ho Chi Minh City, Vietnam

    Phu-Tho Nguyen & Huu-Thanh Nguyen

  4. ProBioLab, Gembloux Agro-Bio Tech, ULiège, Liège, Belgium

    Hary Razafindralambo

  5. Institute of Tropical Biology, Vietnam Academy of Science and Technology, Ho Chi Minh City, Vietnam

    Quoc-Khanh Hoang

Authors
  1. Thi-Tho Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Phu-Tho Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Minh-Nhut Pham
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hary Razafindralambo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Quoc-Khanh Hoang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Huu-Thanh Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Huu-Thanh Nguyen.

Ethics declarations

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nguyen, TT., Nguyen, PT., Pham, MN. et al. Synbiotics: a New Route of Self-production and Applications to Human and Animal Health. Probiotics & Antimicro. Prot. 14, 980–993 (2022). https://doi.org/10.1007/s12602-022-09960-2

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-022-09960-2

Keywords

Search

Navigation