Advertisement

In vitro and in vivo investigations of probiotic properties of lactic acid bacteria isolated from Chinese traditional sourdough

  • Yang Li
  • Tongjie Liu
  • Minjie Zhao
  • Hao Zhong
  • Wenxin Luo
  • Fengqin FengEmail author
Applied microbial and cell physiology

Abstract

A total of 88 lactic acid bacteria (LAB) strains were isolated from Chinese traditional sourdough and five of them were selected based on their bile resistance. All the five strains were identified as Lactobacillus plantarum by 16S rRNA gene sequencing. In vitro probiotic properties of the L. plantarum strains including tolerance to simulated gastrointestinal conditions, aggregation activity, and cholesterol removal ability were assessed. Two representatives, L. plantarum ZJUFT34 and L. plantarum ZJUFT17, were intragastrically administered to male C57BL/6J mice of 4-week age for 6 weeks to evaluate their in vivo health-promoting effects. The results indicated that L. plantarum ZJUFT34, L. plantarum ZJUFHN9, and L. plantarum ZJUFAH5 could survive the 3-h incubation in simulated gastric juice with a pH value of 2.0, while L. plantarum ZJUFT32 and L. plantarum ZJUFT17 exhibited better autoaggregation activities and coaggregation activities with pathogens. All the strains showed a cholesterol removal ability in vitro. However, L. plantarum ZJUFT34 or L. plantarum ZJUFT17 administration did not significantly change the serum total cholesterol in vivo. But the ratio of high-density lipoprotein cholesterol to low-density lipoprotein cholesterol was significantly increased by the L. plantarum administration. Besides, L. plantarum ZJUFT17 significantly lowered serum tumor necrosis factor (TNF)-α concentrations. Furthermore, the administration of the LAB strains showed significant influences on lipid metabolism-related gut microbiota. These findings suggested that the L. plantarum strains may benefit the prevention of metabolic syndrome.

Keywords

Sourdough L. plantarum Serum cholesterol Tumor necrosis factor-α Gut microbiota 

Notes

Funding

This research was supported by the Hangzhou industry-university cooperation project [grant number 20161631E01] and Agricultural Technology Promotion Special Fund of Zhejiang University New Rural Development Institute [grant number 2017006].

Compliance with ethical standards

All institutional and national guidelines for the care and use of laboratory animals were followed.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

253_2018_9554_MOESM1_ESM.pdf (921 kb)
ESM 1 (PDF 920 kb)

References

  1. Angmo K, Kumari A, Savitri BTC (2016) Probiotic characterization of lactic acid bacteria isolated from fermented foods and beverage of Ladakh. Lwt-Food Sci Technol 66:428–435.  https://doi.org/10.1016/j.lwt.2015.10.057 CrossRefGoogle Scholar
  2. Bao Y, Zhang Y, Zhang Y, Liu Y, Wang S, Dong X, Wang Y, Zhang H (2010) Screening of potential probiotic properties of Lactobacillus fermentum isolated from traditional dairy products. Food Control 21:695–701.  https://doi.org/10.1016/j.foodcont.2009.10.010 CrossRefGoogle Scholar
  3. Barreto FM, Simão ANC, Morimoto HK, Lozovoy MAB, Dichi I, da Silva Miglioranza LH (2014) Beneficial effects of Lactobacillus plantarum on glycemia and homocysteine levels in postmenopausal women with metabolic syndrome. Nutrition 30(7–8):939–942CrossRefGoogle Scholar
  4. Bernini LJ, Simão ANC, Alfieri DF, Lozovoy MAB, Mari NL, de Souza CHB, Dichi I, Costa GN (2016) Beneficial effects of Bifidobacterium lactis on lipid profile and cytokines in patients with metabolic syndrome: a randomized trial. Effects of probiotics on metabolic syndrome. Nutrition 32(6):716–719CrossRefGoogle Scholar
  5. Bordoni A, Amaretti A, Leonardi A, Boschetti E, Danesi F, Matteuzzi D, Roncaglia L, Raimondi S, Rossi M (2013) Cholesterol-lowering probiotics: in vitro selection and in vivo testing of bifidobacteria. Appl Microbiol Biotechnol 97(18):8273–8281Google Scholar
  6. Cani PD, Van Hul M (2015) Novel opportunities for next-generation probiotics targeting metabolic syndrome. Curr Opin Biotechnol 32:21–27CrossRefGoogle Scholar
  7. Charteris W, Kelly P, Morelli L, Collins J (1998) Development and application of an in vitro methodology to determine the transit tolerance of potentially probiotic Lactobacillus and Bifidobacterium species in the upper human gastrointestinal tract. J Appl Microbiol 84(5):759–768CrossRefGoogle Scholar
  8. Collado MC, Meriluoto J, Salminen S (2008) Adhesion and aggregation properties of probiotic and pathogen strains. Eur Food Res Technol 226:1065–1073.  https://doi.org/10.1007/s00217-007-0632-x CrossRefGoogle Scholar
  9. Costabile A, Buttarazzi I, Kolida S, Quercia S, Baldini J, Swann JR, Brigidi P, Gibson GR (2017) An in vivo assessment of the cholesterol-lowering efficacy of Lactobacillus plantarum ECGC 13110402 in normal to mildly hypercholesterolaemic adults. PLoS One 12:e0187964.  https://doi.org/10.1371/journal.pone.0187964 CrossRefPubMedPubMedCentralGoogle Scholar
  10. De Vuyst L, Van Kerrebroeck S, Harth H, Huys G, Daniel HM, Weckx S (2014) Microbial ecology of sourdough fermentations: diverse or uniform? Food Microbiol 37:11–29.  https://doi.org/10.1016/j.fm.2013.06.002 CrossRefPubMedGoogle Scholar
  11. Derrien M, Belzer C, de Vos WM (2017) Akkermansia muciniphila and its role in regulating host functions. Microb Pathog 106:171–181.  https://doi.org/10.1016/j.micpath.2016.02.005 CrossRefPubMedGoogle Scholar
  12. Eckel RH, Grundy SM, Zimmet PZ (2005) The metabolic syndrome. Lancet 365(9468):1415–1428CrossRefGoogle Scholar
  13. Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, Guiot Y, Derrien M, Muccioli GG, Delzenne NM, de Vos WM, Cani PD (2013) Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U S A 110(22):9066–9071.  https://doi.org/10.1073/pnas.1219451110 CrossRefPubMedPubMedCentralGoogle Scholar
  14. FAO/WHO (2002) Working group report on drafting guidelines for the evaluation of probiotics in food. Ontario, LondonGoogle Scholar
  15. Feng HW, Pi CM, Wang R, Chen LC (1973) Use of ferric ammonium sulfate in serum-cholesterol determination. Clin Chem 19:121–122PubMedGoogle Scholar
  16. Gobbetti M, Gänzle M (2012) Handbook on sourdough biotechnology. Springer Science & Business MediaGoogle Scholar
  17. Gobbetti M, Minervini F, Pontonio E, Di Cagno R, De Angelis M (2016) Drivers for the establishment and composition of the sourdough lactic acid bacteria biota. Int J Food Microbiol 239:3–18.  https://doi.org/10.1016/j.ifoodmicro.2015.05.022 CrossRefPubMedGoogle Scholar
  18. Guo Z, Wang JC, Yan LY, Chen W, Liu XM, Zhang HP (2009) In vitro comparison of probiotic properties of Lactobacillus casei Zhang, a potential new probiotic, with selected probiotic strains. Lwt-Food Sci Technol 42:1640–1646.  https://doi.org/10.1016/j.lwt.2009.05.025 CrossRefGoogle Scholar
  19. Hotamisligil GkS, Peraldi P, Budavari A, Ellis R, White MF, Spiegelman BM (1996) IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha- and obesity-induced insulin resistance. Science 271(5249):665–670Google Scholar
  20. Kadooka Y, Sato M, Imaizumi K, Ogawa A, Ikuyama K, Akai Y, Okano M, Kagoshima M, Tsuchida T (2010) Regulation of abdominal adiposity by probiotics (Lactobacillus gasseri SBT2055) in adults with obese tendencies in a randomized controlled trial. Eur J Clin Nutr 64(6):636–643CrossRefGoogle Scholar
  21. Kelly TN, Bazzano LA, Ajami NJ, He H, Zhao J, Petrosino JF, Correa A, He J (2016) Gut microbiome associates with lifetime cardiovascular disease risk profile among Bogalusa Heart Study participants. Circ Res 119:956–964.  https://doi.org/10.1161/CIRCRESAHA.116.309219 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Kemp PF, Aller JY (2004) Bacterial diversity in aquatic and other environments: what 16S rDNA libraries can tell us. FEMS Microbiol Ecol 47(2):161–177.  https://doi.org/10.1016/S0168-6496(03)00257-5 CrossRefPubMedGoogle Scholar
  23. Kilic GB, Kuleasan H, Somer VF, Akpinar D (2013) Determining potential probiotic properties of human originated Lactobacillus plantarum strains. Biotechnol Bioproc E 18:479–485.  https://doi.org/10.1007/s12257-012-0785-8 CrossRefGoogle Scholar
  24. Kobayashi T, Taniguchi S, Ye Y, Niekrasz M, Nour B, Cooper DKC (1998) Comparison of bile chemistry between humans, baboons, and pigs: implications for clinical and experimental liver xenotransplantation. Lab Anim Sci 48(2):197–200PubMedGoogle Scholar
  25. LaDuca JR, Gaspari AA (2001) Targeting tumour necrosis factor alpha: new drugs used to modulate inflammatory diseases. Dermatol Clin 19:617–635.  https://doi.org/10.1016/S0733-8635(05)70304-1 CrossRefPubMedGoogle Scholar
  26. Legrand-Defretin V, Juste C, Henry R, Corring T (1991) Ion-pair high-performance liquid chromatography of bile salt conjugates: application to pig bile. Lipids 26(8):578–583CrossRefGoogle Scholar
  27. Liu S-N, Han Y, Z-j Z (2011) Lactic acid bacteria in traditional fermented Chinese foods. Food Res Int 44:643–651.  https://doi.org/10.1016/j.foodres.2010.12.034 CrossRefGoogle Scholar
  28. Liu T, Li Y, Chen J, Sadiq FA, Zhang G, Li Y, He G (2016) Prevalence and diversity of lactic acid bacteria in Chinese traditional sourdough revealed by culture dependent and pyrosequencing approaches. Lwt-Food Sci Technol 68:91–97.  https://doi.org/10.1016/j.lwt.2015.12.025 CrossRefGoogle Scholar
  29. Lu C, Sun T, Li Y, Zhang D, Zhou J, Su X (2018) Microbial diversity and composition in different gut locations of hyperlipidemic mice receiving krill oil. Appl Microbiol Biotechnol 102:355–366.  https://doi.org/10.1007/s00253-017-8601-1 CrossRefPubMedGoogle Scholar
  30. Malik S, Petrova MI, Claes IJJ, Verhoeven TLA, Busschaert P, Vaneechoutte M, Lievens B, Lambrichts I, Siezen RJ, Balzarini J, Vanderleyden J, Lebeer S (2013) The highly autoaggregative and adhesive phenotype of the vaginal Lactobacillus plantarum strain CMPG5300 is sortase dependent. Appl Environ Microbiol 79(15):4576–4585Google Scholar
  31. Manini F, Casiraghi M, Poutanen K, Brasca M, Erba D, Plumed-Ferrer C (2016) Characterization of lactic acid bacteria isolated from wheat bran sourdough. Lwt-Food Sci Technol 66:275–283.  https://doi.org/10.1016/j.lwt.2015.10.045 CrossRefGoogle Scholar
  32. Minami J-I, Kondo S, Yanagisawa N, Odamaki T, Xiao J-z, Abe F, Nakajima S, Hamamoto Y, Saitoh S, Shimoda T (2015) Oral administration of Bifidobacterium breve B-3 modifies metabolic functions in adults with obese tendencies in a randomised controlled trial. J Nutr Sci 4Google Scholar
  33. Papadimitriou K, Zoumpopoulou G, Foligne B, Alexandraki V, Kazou M, Pot B, Tsakalidou E (2015) Discovering probiotic microorganisms: in vitro, in vivo, genetic and omics approaches. Front Microbiol 6:58.  https://doi.org/10.3389/fmicb.2015.00058 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Pena JA, Versalovic J (2003) Lactobacillus rhamnosus GG decreases TNF-α production in lipopolysaccharide-activated murine macrophages by a contact-independent mechanism. Cell Microbiol 5:277–285.  https://doi.org/10.1046/j.1462-5822.2003.t01-1-00275.x CrossRefPubMedGoogle Scholar
  35. Ramos CL, Thorsen L, Schwan RF, Jespersen L (2013) Strain-specific probiotics properties of Lactobacillus fermentum, Lactobacillus plantarum and Lactobacillus brevis isolates from Brazilian food products. Food Microbiol 36:22–29.  https://doi.org/10.1016/j.fm.2013.03.010 CrossRefGoogle Scholar
  36. Sanchez B, Delgado S, Blanco-Miguez A, Lourenco A, Gueimonde M, Margolles A (2017) Probiotics, gut microbiota, and their influence on host health and disease. Mol Nutr Food Res 61(1).  https://doi.org/10.1002/mnfr.201600240
  37. Sekiguchi H, Kawada-Watanabe E, Arashi H, Yamaguchi J, Ogawa H, Hagiwara N (2018) Association between the low-density lipoprotein-cholesterol/high-density lipoprotein-cholesterol ratio and clinical outcomes in patients with acute coronary syndrome and dyslipidemia: a subanalysis of the HIJ-PROPER study. J Am Coll Cardiol 71:A1757.  https://doi.org/10.1016/S0735-1097(18)32298-8 CrossRefGoogle Scholar
  38. Shang Q, Song G, Zhang M, Shi J, Xu C, Hao J, Li G, Yu G (2017) Dietary fucoidan improves metabolic syndrome in association with increased Akkermansia population in the gut microbiota of high-fat diet-fed mice. J Funct Foods 28:138–146.  https://doi.org/10.1016/j.jff.2016.11.002 CrossRefGoogle Scholar
  39. Suez J, Zmora N, Zilberman-Schapira G, Mor U, Dori-Bachash M, Bashiardes S, Zur M, Regev-Lehavi D, Ben-Zeev Brik R, Federici S, Horn M, Cohen Y, Moor AE, Zeevi D, Korem T, Kotler E, Harmelin A, Itzkovitz S, Maharshak N, Shibolet O, Pevsner-Fischer M, Shapiro H, Sharon I, Halpern Z, Segal E, Elinav E (2018) Post-antibiotic gut mucosal microbiome reconstitution is impaired by probiotics and improved by autologous FMT. Cell 174(6):1406–1423 e16.  https://doi.org/10.1016/j.cell.2018.08.047 CrossRefPubMedGoogle Scholar
  40. Tan Q, Xu H, Aguilar ZP, Peng S, Dong S, Wang B, Li P, Chen T, Xu F, Wei H (2013) Safety assessment and probiotic evaluation of Enterococcus faecium YF5 isolated from sourdough. J Food Sci 78:M587–M593.  https://doi.org/10.1111/1750-3841.12079 CrossRefPubMedGoogle Scholar
  41. Thornton GM (1996) Probiotic bacteria: selection of Lactobacillus and Bifidobacterium strains from the healthy human gastrointestinal tract; characterisation of a novel Lactobacillus-derived antibacterial protein. NUIGoogle Scholar
  42. Trivedi D, Jena PK, Patel JK, Seshadri S (2013) Partial purification and characterization of a bacteriocin DT24 produced by probiotic vaginal Lactobacillus brevis DT24 and determination of its anti-uropathogenic Escherichia coli potential. Probiotics Antimicrob 5:142–151.  https://doi.org/10.1007/s12602-013-9132-4 CrossRefGoogle Scholar
  43. Tse MCL, Herlea-Pana O, Brobst D, Yang X, Wood J, Hu X, Liu Z, Lee CW, Zaw AM, Chow BKC, Ye K, Chan CB (2017) Tumor necrosis factor-alpha promotes phosphoinositide 3-kinase enhancer a and AMP-activated protein kinase interaction to suppress lipid oxidation in skeletal muscle. Diabetes 66:1858–1870.  https://doi.org/10.2337/db16-0270 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Walker DK, Gilliland SE (1993) Relationships among bile tolerance, bile salt deconjugation, and assimilation of cholesterol by Lactobacillus acidophilus. J Dairy Sci 76(4):956–961Google Scholar
  45. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173(2):697–703CrossRefGoogle Scholar
  46. Yang D, Yu X, Wu Y, Chen X, Wei H, Shah NP, Xu F (2016) Enhancing flora balance in the gastrointestinal tract of mice by lactic acid bacteria from Chinese sourdough and enzyme activities indicative of metabolism of protein, fat, and carbohydrate by the flora. J Dairy Sci 99(10):7809–7820CrossRefGoogle Scholar
  47. Zmora N, Zilberman-Schapira G, Suez J, Mor U, Dori-Bachash M, Bashiardes S, Kotler E, Zur M, Regev-Lehavi D, Brik RB, Federici S, Cohen Y, Linevsky R, Rothschild D, Moor AE, Ben-Moshe S, Harmelin A, Itzkovitz S, Maharshak N, Shibolet O, Shapiro H, Pevsner-Fischer M, Sharon I, Halpern Z, Segal E, Elinav E (2018) Personalized gut mucosal colonization resistance to empiric probiotics is associated with unique host and microbiome features. Cell 174(6):1388–1405 e21.  https://doi.org/10.1016/j.cell.2018.08.041 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Yang Li
    • 1
    • 2
  • Tongjie Liu
    • 3
  • Minjie Zhao
    • 1
    • 2
  • Hao Zhong
    • 1
    • 2
  • Wenxin Luo
    • 1
  • Fengqin Feng
    • 1
    • 2
  1. 1.College of Biosystems Engineering and Food ScienceZhejiang UniversityHangzhouChina
  2. 2.Zhejiang Key Laboratory for Agro-Food ProcessingZhejiang UniversityHangzhouChina
  3. 3.College of Food Science and EngineeringOcean University of ChinaQingdaoChina

Personalised recommendations