Abstract
In this study, it was aimed to reveal the potential of using exopolysaccharides (EPS) obtained from Ligilactobacillus salivarius as a prebiotic that regulates chicken intestinal microbiota. Characterization of EPS obtained from L. salivarius BIS312 (EPSBIS312) and BIS722 (EPSBIS722) strains was demonstrated by high performance liquid chromatography (HPLC), nuclear magnetic resonance (NMR), and size-exclusion chromatography (SEC) analyses. It was determined that the molecular weight of both EPS is in the range of 104–106 Daltons, and there are 4 types of monomers in their structure. Anti-biofilm and anti-quorum sensing effects of EPSBIS312 and EPSBIS722 were determined. EPSBIS312 and EPSBIS722 showed a strong anti-biofilm effect on Enterococcus faecalis ATCC 29212, Staphylococcus aureus EB-1, and Escherichia coli ATCC 11229. The anti-quorum sensing study revealed that the EPSBIS722 had a higher effect than the EPSBIS312. The effect of different concentrations of EPS (2.5%, 5%, 10%) on lactobacilli growth stimulator (LGS) was evaluated. The highest LGS was promoted at 10% concentration while the lowest LGS was promoted at 2.5% concentration by EPSBIS722. In addition, adhesion abilities of EPSBIS312 and EPSBIS722 in HT-29 colorectal adenocarcinoma cell line were tested. EPSs significantly increased the ability to adhere to HT-29 cells. The characterized EPSs may be an alternative to plant prebiotics such as inulin at poultry.
Similar content being viewed by others
Availability of Data and Materials
The data that support the findings of this study are available from the corresponding author on request.
References
Pourabedin M, Zhao X (2015) Prebiotics and gut microbiota in chickens. FEMS MicrobiolLett 362(15):1–14. https://doi.org/10.1093/femsle/fnv122
Baldwin S, Hughes RJ, Van TTH, Moore RJ, Stanley D (2018) At-hatch administration of probiotic to chickens can introduce beneficial changes in gut microbiota. PLoS ONE 13(3):1–14. https://doi.org/10.1371/journal.pone.0194825
Ahmed Z, Vohra MS, Khan MN, Ahmed A, Khan TA (2019) Antimicrobial role of Lactobacillus species as potential probiotics against enteropathogenic bacteria in chickens. J Infect Dev Count 13(2):130–136. https://doi.org/10.3855/jidc.10542
Pfaller MA (2006) Flavophospholipol use in animals: positive implications for antimicrobial resistance based on its microbiologic properties. DiagnMicrobiol Infect Dis 56(2):115–121. https://doi.org/10.1016/j.diagmicrobio.2006.03.014
Peebles ED (2018) In ovo applications in poultry: a review. PoultSci 97(7):2322–2338. https://doi.org/10.3382/ps/pey081
Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB et al (2014) The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev GastroenterolHepatol 11:506–514. https://doi.org/10.1038/nrgastro.2014.66
Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C et al (2017) The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nature Rev|Gastroenterol Hepatol 14:491–502. https://doi.org/10.1038/nrgastro.2017.75
Kareem KY, Loh TC, Foo HL, Akit H, Samsudin AA (2016) Effects of dietary postbiotic and inulin on growth performance, IGF1 and GHR mRNA expression, faecal microbiota and volatile fatty acids in broilers. BMC Vet Res 12(1):163. https://doi.org/10.1186/s12917-016-0790-9
Jahromi MF, Altaher YW, Shokryazdan P, Ebrahimi R, Ebrahimi M, Idru Z, Tufarelli V, Liang JB (2016) Dietary supplementation of a mixture of Lactobacillus strains enhances performance of broiler chickens raised under heat stress conditions. Int J Biometeorol 60(7):1099–1110. https://doi.org/10.1007/s00484-015-1103-x
Zheng J, Wittouck S, Salvetti E, Franz CMAP, Harris HMB, Mattarelli P, Toole PWO, Pot B, Vandamme P, Walter J et al (2020) A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus LactobacillusBeijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int J SystEvolMicrobiol 70:2782–2858. https://doi.org/10.1099/ijsem.0.004107
Yi Y, Huang W, Ge Y (2008) Exopolysaccharide: a novel important factor in the microbial dissolution of tricalcium phosphate. World J MicrobiolBiotechnol 24(7):1061. https://doi.org/10.1007/s11274-007-9575-4
Kanmani P, Yuvaraj N, Paari KA, Pattukumar V, Arul V (2011) Production and purification of a novel exopolysaccharide from lactic acid bacterium Streptococcus phocae PI80 and its functional characteristics activity in vitro. BioresourTechnol 102(7):4827–4833. https://doi.org/10.1016/j.biortech.2010.12.118
Ledezma OEV, Méndez HIP, Maldonado LÁ, Manjarrez ETQC, Alvarez NM, López-Luna A (2016) Characterization of extracellular polymeric substances (EPS) produced by marine Micromonospora sp. J Chem Pharm Res 8(7):442–451. ISSN: 0975–7384
Ismail B, MadhavanNampoothiri K (2013) Exposition of antitumour activity of a chemically characterized exopolysaccharide from a probiotic Lactobacillus plantarum MTCC 9510. Biol Sect Cell MolBiol 68:1041–1047. https://doi.org/10.2478/s11756-013-0275-2
Stepanović S, Vuković D, Dakić I, Savić B, Švabić-Vlahović M (2000) A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods 40(2):175–179. https://doi.org/10.1016/S0167-7012(00)00122-6
Jagani S, Chelikani R, Kim DS (2009) Effects of phenol and natural phenolic compounds on biofilm formation by Pseudomonas aeruginosa. Biofouling 25(4):321–324. https://doi.org/10.1080/08927010802660854
Chaieb K, Kouidhi B, Jrah H, Mahdouani K, Bakhrouf A (2011) Antibacterial activity of thymoquinone, an active principle of Nigella sativa and its potency to prevent bacterial biofilm formation. BMC Complement Altern Med 11(1):29. https://doi.org/10.1186/1472-6882-11-29
Choo JH, Rukayadi Y, Hwan JK (2006) Inhibition of bacterial quorum sensing by vanilia extract. LettApplMicrobiol 42:637–641. https://doi.org/10.1111/j.1472-765X.2006.01928.x
Tsuda H, Okuda S, Haraguchi T, Kodama K (2018) Influence of exopolysaccharide on the growth of lactic acid bacteria. Ital J Food Sci 31(2):10–17. https://doi.org/10.14674/IJFS-1317
Jacobsen CN, Nielsen VR, Hayford AE, Møller PL, Michaelsen KF, Paerregaard A, Sandström B, Tvede M, Jakobsen M (1999) Screening of probiotic activities of forty-seven strains of Lactobacillus spp. by in vitro techniques and evaluation of the colonization ability of five selected strains in humans. Appl Environ Microbiol 65(11):4949–4956. https://doi.org/10.1128/AEM.65.11.4949-4956.1999
Otero MC, Nader-Macías ME (2007) Lactobacillus adhesion to epithelial cells from bovine vagina. Com Curr Res Edu Top Trends Appl Microbiol 749–757.
Santagati M, Scillato M, Patanè F, Aiello C, Stefani S (2012) Bacteriocin-producing oral streptococci and inhibition of respiratory pathogens. FEMS Immunol Med Microbiol 65(1):23–31. https://doi.org/10.1111/j.1574-695X.2012.00928.x
Hu X, Li D, Qiao Y, Wang X, Zhang Q, Zhao W, Huang L (2020) Purification, characterization and anticancer activities of exopolysaccharide produced by Rhodococcus erythropolis HX-2. Int J BiolMacromol 145:646–654. https://doi.org/10.1016/j.ijbiomac.2019.12.228
Iliev I, Ivanova I, Ignatova C (2006) Glucansucrases from lactic acid bacteria (LAB). BiotechnolBiotechnol Equip 20(3):15–20. https://doi.org/10.1080/13102818.2006.10817374
Xu Z, Guo Q, Zhang H, Wu Y, Hang X, Ai L (2018) Exopolysaccharide produced by Streptococcus thermophiles S-3: molecular, partial structural and rheological properties. CarbohydrPolym 194:132–138. https://doi.org/10.1016/j.carbpol.2018.04.014
Liu T, Zhou K, Yin S, Liu S, Zhu Y, Yang Y, Wang C (2019) Purification and characterization of an exopolysaccharide produced by Lactobacillus plantarum HY isolated from home-made Sichuan Pickle. Int J BiolMacromol 134:516–526. https://doi.org/10.1016/j.ijbiomac.2019.05.010
Nordmark EL (2004) Structural and interaction studies of bacterial polysaccharides by NMR spectroscopy. (Stockholm University) Printed in Sweden by Akademitryck AB Valdemarsvik 1–50. ISBN 91–7265–971–8.
Zhou K, Zeng Y, Yang M, Chen S, He L, Ao X, Zou L, Liu S (2016) Production, purification, and structural study of an exopolysaccharide from Lactobacillus plantarum BC-25. CarbohydrPolym 144:205–214. https://doi.org/10.1016/j.carbpol.2016.02.067
Wang J, Zhao X, Tian Z, Yang Y, Yang Z (2015) Characterization of an exopolysaccharide produced by Lactobacillus plantarum YW11 isolated from Tibet Kefir. CarbohydrPolym 125:16–25. https://doi.org/10.1016/j.carbpol.2015.03.003
Jiang Y, Yang Z (2018) A functional and genetic overview of exopolysaccharides produced by Lactobacillus plantarum. J Funct Foods 47229:240. https://doi.org/10.1016/j.jff.2018.05.060
Wang J, Zhao X, Tian Z, He C, Yang Y, Yang Z (2015) Isolation and characterization of exopolysaccharide-producing Lactobacillus plantarum SKT109 from Tibet Kefir. Pol J Food NutrSci 65(4):269–280. https://doi.org/10.1515/pjfns-2015-0023
Garde C, Welch M, Ferkinghoff-Borg J, Sams T (2015) Microbial biofilm as a smart material. Sensors 15(2):4229–4241. https://doi.org/10.3390/s150204229
Kim Y, Oh S, Kim SH (2009) Released exopolysaccharide (r-EPS) produced from probiotic bacteria reduce biofilm formation of enterohemorrhagicEscherichia coli O157: H7. BiochemBiophys Res Commun 379(2):324–329. https://doi.org/10.1016/j.bbrc.2008.12.053
Wang K, Niu M, Song D, Song X, Zhao J, Wu Y, Lu B, Niu G (2020) Preparation, partial characterization and biological activity of exopolysaccharides produced from Lactobacillus fermentum S1. J BiosciBioengin 129(2):206–214. https://doi.org/10.1016/j.jbiosc.2019.07.009
Huang J, Yi K, Zeng G, Shi Y, Gu Y, Shi L, Yu H (2019) The role of quorum sensing in granular sludge: Impact and future application: a review. Chemosphere 236:124310. https://doi.org/10.1016/j.chemosphere.2019.07.041
Choo JH, Rukayadi Y, Hwang JK (2006) Inhibition of bacterial quorum sensing by vanilla extract. LettApplMicrobiol 42(6):637–641. https://doi.org/10.1111/j.1472-765X.2006.01928.x
Sugiharto S (2016) Role of nutraceuticals in gut health and growth performance of poultry. J Saudi SocAgric 15(2):99–111. https://doi.org/10.1016/j.jssas.2014.06.001
Shang Y, Kumar S, Thippareddi H, Kim WK (2018) Effect of dietary fructooligosaccharide (FOS) supplementation on ilealmicrobiota in broiler chickens. PoultSci 97(10):3622–3634. https://doi.org/10.3382/ps/pey131
Di Gioia D, Biavati B (2018) Probiotics and prebiotics in animal health and food safety: conclusive remarks and future perspectives. Probiotics Prebiotics Animal Health Food Safe 4(11):269–273. https://doi.org/10.1007/978-3-319-71950-4_11
Tarabees R, Gafar KM, EL-Sayed MS, Shehata AA, Ahmed M (2018) Effects of dietary supplementation of probiotic mix and prebiotic on growth performance, cecalmicrobiota composition, and protection against Escherichia coli O78 in broiler chickens. Probiotics Antimicrob Proteins 10:1–9. https://doi.org/10.1007/s12602-018-9459-y
Sarikaya H, Aslim B, Yuksekdag ZN (2017) Assessment of anti-biofilm activity and bifidogenic growth stimulator (BGS) effect of lyophilized exopolysaccharides (l-EPSs) from Lactobacilli strains. Int J Food Prop 20:362–371. https://doi.org/10.1080/10942912.2016.1160923
Nakphaichit M, Thanomwongwattana S, Phraephaisarn C, Sakamoto N, Keawsompong S, Nakayama J, Nitisinprasert S (2011) The effect of including Lactobacillus reuteri KUB-AC5 during post-hatch feeding on the growth and ileum microbiota of broiler chickens. PoultSci 90(12):2753–2765. https://doi.org/10.3382/ps.2011-01637
Mappley LJ, Tchórzewska MA, Nunez A, Woodward MJ, Bramley PM, La Ragione RM (2013) Oral treatment of chickens with Lactobacillus reuteri LM1 reduces Brachyspirapilosicoli-induced pathology. J Med Microbiol 62(2):287–296. https://doi.org/10.1099/jmm.0.051862-0
Huebner J, Wehling RL, Hutkins RW (2007) Functional activity of commercial prebiotics. Int Dairy J 17:770–775. https://doi.org/10.1016/j.idairyj.2006.10.006
Tsuda H, Miyamoto T (2010) Production of exopolysaccharide by Lactobacillus plantarum and the prebiotic activity of the exopolysaccharide. Food SciTechnol Res 16(1):87–92. https://doi.org/10.3136/fstr.16.87
Muñoz-Provencio D, Llopis M, Antolín M, De Torres I, Guarner F, Pérez-Martínez G, Monedero V (2009) Adhesion properties of Lactobacillus casei strains to resected intestinal fragments and components of the extracellular matrix. Arch Microbiol 191(2):153–161. https://doi.org/10.1007/s00203-008-0436-9
Zivkovic M, Miljkovic MS, Ruas-Madiedo P, Markelic MB, Veljovic K, Tolinacki M, Sokovic S, Korac A, Golic N (2016) EPS-SJ exopolisaccharide produced by the strain Lactobacillus paracasei subsp. paracasei BGSJ2–8 is involved in adhesion to epithelial intestinal cells and decrease on E. coli association to Caco-2 cells. Front Microbiol 7:286. https://doi.org/10.3389/fmicb.2016.00286
Gupta A, Sharma N (2015) Assessment of cell surface properties and adhesion potential of lactic acid bacteria isolated from Lasodabari-A rare, fermented food of Himachal Pradesh. Eur J BiotechnolBiosci 3(8):9–15. https://doi.org/10.1111/j.1472-765X.2009.02684.x
Acknowledgements
The authors thanks Republic of Turkey Ministry of Agriculture and Forestry General Directorate of Agricultural Research and Policies (TAGEM/15/AR-GE/40) for financial supporting.
Funding
The authors would like to thank Republic of Turkey Ministry of Agriculture and Forestry General Directorate of Agricultural Research and Policies for funding the TAGEM/15/AR-GE/40 coded project including this study.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Compliance with Ethics Requirements
This article does not contain any studies with human or animal subjects.
Competing Interests
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
About this article
Cite this article
Bikric, S., Aslim, B., Dincer, İ. et al. Characterization of Exopolysaccharides (EPSs) Obtained from Ligilactobacillus salivarius Strains and Investigation at the Prebiotic Potential as an Alternative to Plant Prebiotics at Poultry. Probiotics & Antimicro. Prot. 14, 49–59 (2022). https://doi.org/10.1007/s12602-021-09790-8
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12602-021-09790-8