Skip to main content

Advertisement

SpringerLink
Log in

Probiotic Features of Lactic Acid Bacteria Isolated from a Diverse Pool of Traditional Greek Dairy Products Regarding Specific Strain-Host Interactions

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

Abstract

The increased consumers’ interest on the positive role of food in wellbeing and health underscores the need to determine new probiotic microorganisms. Triggered by the fact that artisanal food products can be a valuable source of novel probiotic strains, 106 lactic acid bacteria, all isolated from traditional Greek dairy products, namely Feta, Kasseri, Xynotyri, Graviera, Formaela, Galotyri, and Kefalotyri cheeses as well as yogurt and milk, were studied for probiotic properties. Based on their survival at pH 2.5 and their stability in the presence of bile salts, 20 strains were selected for further analysis. These strains exhibited diverse susceptibility to commonly used antibiotics, while none was hemolytic. Seven out of the 20 strains produced functional bile salt hydrolases in vitro. The only antimicrobial activity detected of Streptococcus thermophilus ACA-DC 26 against the oral pathogen Streptococcus mutans LMG 14558T was attributed to compound(s) of proteinaceous nature. Two Lactobacillus plantarum strains, namely ACA-DC 2640 and ACA-DC 4039, displayed the highest adhesion according to a collagen-based microplate assay and by using ΗΤ-29 and Caco-2 cells. Co-cultivation of THP-1 cells with selected strains indicated a tendency for anti-inflammatory modulation by Lactobacillus plantarum ACA-DC 2640 as well as Streptococcus thermophilus ACA-DC 26 and ACA-DC 170, as shown by an increase in IL10 mRNA levels. Moreover, milk cell-free supernatants of Lactobacillus plantarum ACA-DC 2640 and ACA-DC 4039 exhibited strong angiotensin I-converting enzyme inhibition. To conclude, new isolates presenting interesting probiotic features were described and should be further investigated as health-promoting factors.

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

Similar content being viewed by others

References

  1. Thomas LV (2016) Probiotics—the journey continues. Int J Dairy Technol 69(4):469–480. doi:10.1111/1471-0307.12354

    Article  CAS  Google Scholar 

  2. Zoumpopoulou G, Pot B, Tsakalidou E, Papadimitriou K (2017) Dairy probiotics: beyond the role of promoting gut and immune health. Int Dairy J 67:46–60. doi:10.1016/j.idairyj.2016.09.010

    Article  Google Scholar 

  3. Santos TT, Ornellas RMS, Arcucio LB, Oliveira MM, Nicoli JR, Dias CV, Uetanabaro APT, Vinderola G (2016) Characterization of lactobacilli strains derived from cocoa fermentation in the south of Bahia for the development of probiotic cultures. LWT Food Sci Technol 73:259–266. doi:10.1016/j.lwt.2016.06.003

    Article  CAS  Google Scholar 

  4. Regulation (EC) No 1924/2006 of the European Parliament and of the Council of 20 December 2006 on nutrition and health claims made on foods. Off J Eur Union L12:3–18

  5. Italian Ministry of Health (2013) Guidelines on probiotics and prebiotics. Internet document URL http://www.salute.gov.it/imgs/C_17_pubblicazioni_1016_ulterioriallegati_ulterioreallegato_0_alleg.pdf

  6. Papadimitriou K, Zoumpopoulou G, Foligné 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. doi:10.3389/fmicb.2015.00058

    Article  PubMed  PubMed Central  Google Scholar 

  7. Litopoulou-Tzanetaki E, Tzanetakis N (2011) Microbiological characteristics of Greek traditional cheeses. Small Rumin Res 101(1–3):17–32. doi:10.1016/j.smallrumres.2011.09.022

    Article  Google Scholar 

  8. Zoumpopoulou G, Foligne B, Christodoulou K, Grangette C, Pot B, Tsakalidou E (2008) Lactobacillus fermentum ACA-DC 179 displays probiotic potential in vitro and protects against trinitrobenzene sulfonic acid (TNBS)-induced colitis and Salmonella infection in murine models. Int J Food Microbiol 121(1):18–26. doi:10.1016/j.ijfoodmicro.2007.10.013

    Article  CAS  PubMed  Google Scholar 

  9. Tram G, Korolik V, Day CJ (2013) MBDS solvent: an improved method for assessment of biofilms. Adv Microbiol 3:200–204. doi:10.4236/aim.2013.32030

    Article  CAS  Google Scholar 

  10. Siegesmund AM, Konkel ME, Klena JD, Mixter PF (2004) Campylobacter jejuni infection of differentiated THP-1 macrophages results in interleukin 1β release and caspase-1-independent apoptosis. Microbiol 150(3):561–569. doi:10.1099/mic.0.26466-0

    Article  CAS  Google Scholar 

  11. Dimozi A, Mavrogonatou E, Sklirou A, Kletsas D (2015) Oxidative stress inhibits the proliferation, induces premature senescence and promotes a catabolic phenotype in human nucleus pulposus intervertebral disc cells. Eur Cell Mater 30:89–102; discussion 103. doi:10.22203/eCM.v030a07

    Article  CAS  PubMed  Google Scholar 

  12. Muguerza B, Ramos M, Sánchez E, Manso MA, Miguel M, Aleixandre A, Delgado MA, Recio I (2006) Antihypertensive activity of milk fermented by Enterococcus faecalis strains isolated from raw milk. Int Dairy J 16(1):61–69. doi:10.1016/j.idairyj.2005.01.001

    Article  CAS  Google Scholar 

  13. Quirós A, Ramos M, Muguerza B, Delgado MA, Miguel M, Aleixandre A, Recio I (2007) Identification of novel antihypertensive peptides in milk fermented with Enterococcus faecalis. Int Dairy J 17(1):33–41. doi:10.1016/j.idairyj.2005.12.011

    Article  CAS  Google Scholar 

  14. Pan D, Luo Y, Tanokura M (2005) Antihypertensive peptides from skimmed milk hydrolysate digested by cell-free extract of Lactobacillus helveticus JCM1004. Food Chem 91(1):123–129. doi:10.1016/j.foodchem.2004.05.055

    Article  CAS  Google Scholar 

  15. EFSA (2012) Guidance on the assessment of bacterial susceptibility to antimicrobials of human and veterinary importance. EFSA J 10(6):2740-n/a. doi:10.2903/j.efsa.2012.2740

    Article  CAS  Google Scholar 

  16. Amund OD (2016) Exploring the relationship between exposure to technological and gastrointestinal stress and probiotic functional properties of lactobacilli and bifidobacteria. Can J Microbiol 62(9):715–725. doi:10.1139/cjm-2016-0186

    Article  CAS  PubMed  Google Scholar 

  17. Devirgiliis C, Barile S, Perozzi G (2011) Antibiotic resistance determinants in the interplay between food and gut microbiota. Genes Nutr 6(3):275–284. doi:10.1007/s12263-011-0226-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Gueimonde M, Sanchez B, GdLR-G C, Margolles A (2013) Antibiotic resistance in probiotic bacteria. Front Microbiol 4:202. doi:10.3389/fmicb.2013.00202

    Article  PubMed  PubMed Central  Google Scholar 

  19. Salvetti E, Orrù L, Capozzi V, Martina A, Lamontanara A, Keller D, Cash H, Felis GE, Cattiveli L, Torriani S, Spano G (2016) Integrate genome-based assessment of safety for probiotic strains: Bacillus coagulans GBI-30, 6086 as a case study. Appl Microbiol Biotechnol 100(10):4595–4605. doi:10.1007/s00253-016-7416-9

    Article  CAS  PubMed  Google Scholar 

  20. de Moraes GMD, de Abreu LR, do Egito AS, Salles HO, da Silva LMF, Nero LA, Todorov SD, dos Santos KMO (2016) Functional properties of Lactobacillus mucosae strains isolated from Brazilian goat milk. Probiotics Antimicrob Proteins 1–11. doi:10.1007/s12602-016-9244-8

  21. Ouwehand AC, Forssten S, Hibberd AA, Lyra A, Stahl B (2016) Probiotic approach to prevent antibiotic resistance. Ann Med 48(4):246–255. doi:10.3109/07853890.2016.1161232

    Article  CAS  PubMed  Google Scholar 

  22. Ammor MS, Florez AB, Mayo B (2007) Antibiotic resistance in non-enterococcal lactic acid bacteria and bifidobacteria. Food Microbiol 24(6):559–570. doi:10.1016/j.fm.2006.11.001

    Article  CAS  PubMed  Google Scholar 

  23. Bernardeau M, Vernoux JP, Henri-Dubernet S, Guéguen M (2008) Safety assessment of dairy microorganisms: the Lactobacillus genus. Int J Food Microbiol 126(3):278–285. doi:10.1016/j.ijfoodmicro.2007.08.015

    Article  CAS  PubMed  Google Scholar 

  24. Guidone A, Zotta T, Ross RP, Stanton C, Rea MC, Parente E, Ricciardi A (2014) Functional properties of Lactobacillus plantarum strains: a multivariate screening study. LWT Food Sci Technol 56(1):69–76. doi:10.1016/j.lwt.2013.10.036

    Article  CAS  Google Scholar 

  25. Nawaz M, Wang J, Zhou A, Ma C, Wu X, Moore JE, Millar BC, Xu J (2011) Characterization and transfer of antibiotic resistance in lactic acid bacteria from fermented food products. Curr Microbiol 62(3):1081–1089. doi:10.1007/s00284-010-9856-2

    Article  CAS  PubMed  Google Scholar 

  26. Hashemi SM, Shahidi F, Mortazavi SA, Milani E, Eshaghi Z (2014) Potentially probiotic Lactobacillus strains from traditional Kurdish cheese. Probiotics Antimicrob Proteins 6(1):22–31. doi:10.1007/s12602-014-9155-5

    Article  CAS  PubMed  Google Scholar 

  27. Chand D, Avinash VS, Yadav Y, Pundle AV, Suresh CG, Ramasamy S (2017) Molecular features of bile salt hydrolases and relevance in human health. Biochim Biophys Acta 1861:2981–2991. doi:10.1016/j.bbagen.2016.09.024

    Article  CAS  Google Scholar 

  28. Joyce SA, Shanahan F, Hill C, Gahan CG (2014) Bacterial bile salt hydrolase in host metabolism: potential for influencing gastrointestinal microbe-host crosstalk. Gut Microbes 5(5):669–674. doi:10.4161/19490976.2014.969986

    Article  PubMed  PubMed Central  Google Scholar 

  29. Begley M, Hill C, Gahan CG (2006) Bile salt hydrolase activity in probiotics. Appl Environ Microbiol 72(3):1729–1738. doi:10.1128/aem.72.3.1729-1738.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Lv LX, Yan R, Shi HY, Shi D, Fang DQ, Jiang HY, Wu WR, Guo FF, Jiang XW, Gu SL, Chen YB, Yao J, Li LJ (2017) Integrated transcriptomic and proteomic analysis of the bile stress response in probiotic Lactobacillus salivarius LI01. J Proteome 150:216–229. doi:10.1016/j.jprot.2016.08.021

    Article  CAS  Google Scholar 

  31. Patel AK, Singhania RR, Pandey A, Chincholkar SB (2010) Probiotic bile salt hydrolase: current developments and perspectives. Appl Biochem Biotechnol 162(1):166–180. doi:10.1007/s12010-009-8738-1

    Article  CAS  PubMed  Google Scholar 

  32. Archer AC, Halami PM (2015) Probiotic attributes of Lactobacillus fermentum isolated from human feces and dairy products. Appl Microbiol Biotechol 99(19):8113–8123. doi:10.1007/s00253-015-6679-x

    Article  CAS  Google Scholar 

  33. Vizoso Pinto MG, Franz CM, Schillinger U, Holzapfel WH (2006) Lactobacillus spp. with in vitro probiotic properties from human faeces and traditional fermented products. Int J Food Microbiol 109(3):205–214. doi:10.1016/j.ijfoodmicro.2006.01.029

    Article  CAS  PubMed  Google Scholar 

  34. Miquel S, Beaumont M, Martin R, Langella P, Braesco V, Thomas M (2015) A proposed framework for an appropriate evaluation scheme for microorganisms as novel foods with a health claim in Europe. Microb Cell Factories 14:48. doi:10.1186/s12934-015-0229-1

    Article  CAS  Google Scholar 

  35. Reid G, Younes JA, Van der Mei HC, Gloor GB, Knight R, Busscher HJ (2011) Microbiota restoration: natural and supplemented recovery of human microbial communities. Nat Rev Microbiol 9(1):27–38. doi:10.1038/nrmicro2473

    Article  CAS  PubMed  Google Scholar 

  36. Zoumpopoulou G, Pepelassi E, Papaioannou W, Georgalaki M, Maragkoudakis PA, Tarantilis PA, Polissiou M, Tsakalidou E, Papadimitriou K (2013) Incidence of bacteriocins produced by food-related lactic acid bacteria active towards oral pathogens. Int J Mol Sci 14(3):4640–4654. doi:10.3390/ijms14034640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Bermudez-Brito M, Plaza-Diaz J, Munoz-Quezada S, Gomez-Llorente C, Gil A (2012) Probiotic mechanisms of action. Ann Nutr Metab 61(2):160–174. doi:10.1159/000342079

    Article  CAS  PubMed  Google Scholar 

  38. Sengupta R, Altermann E, Anderson RC, McNabb WC, Moughan PJ, Roy NC (2013) The role of cell surface architecture of lactobacilli in host-microbe interactions in the gastrointestinal tract. Mediat Inflamm 2013:16. doi:10.1155/2013/237921

    Article  Google Scholar 

  39. Fabien JC, Stephanie-Marie D, Adriana Perez C, Benoit F, Gwenael J (2012) Interactions between probiotic dairy propionibacteria and the intestinal epithelium. Curr Immunol Rev 8(3):216–226. doi:10.2174/157339512800671976

    Article  Google Scholar 

  40. Lievin-Le Moal V, Servin AL (2013) Pathogenesis of human enterovirulent bacteria: lessons from cultured, fully differentiated human colon cancer cell lines. Microbiol Mol Biol Rev 77(3):380–439. doi:10.1128/mmbr.00064-12

    Article  PubMed  PubMed Central  Google Scholar 

  41. Gagnon M, Zihler Berner A, Chervet N, Chassard C, Lacroix C (2013) Comparison of the Caco-2, HT-29 and the mucus-secreting HT29-MTX intestinal cell models to investigate Salmonella adhesion and invasion. J Microbiol Methods 94(3):274–279. doi:10.1016/j.mimet.2013.06.027

    Article  CAS  PubMed  Google Scholar 

  42. Wang B, Wei H, Yuan J, Li Q, Li Y, Li N, Li J (2008) Identification of a surface protein from Lactobacillus reuteri JCM1081 that adheres to porcine gastric mucin and human enterocyte-like HT-29 cells. Curr Microbiol 57(1):33–38. doi:10.1007/s00284-008-9148-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Laparra JM, Sanz Y (2009) Comparison of in vitro models to study bacterial adhesion to the intestinal epithelium. Lett Appl Microbiol 49(6):695–701. doi:10.1111/j.1472-765X.2009.02729.x

    Article  CAS  PubMed  Google Scholar 

  44. Mosser DM, Edwards JP (2008) Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8(12):958–969. doi:10.1038/nri2448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Qin Z (2012) The use of THP-1 cells as a model for mimicking the function and regulation of monocytes and macrophages in the vasculature. Atherosclerosis 221(1):2–11. doi:10.1016/j.atherosclerosis.2011.09.003

    Article  CAS  PubMed  Google Scholar 

  46. Cassetta L, Cassol E, Poli G (2011) Macrophage polarization in health and disease. Sci World J 11:2391–2402. doi:10.1100/2011/213962

    Article  CAS  Google Scholar 

  47. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25(12):677–686. doi:10.1016/j.it.2004.09.015

    Article  CAS  PubMed  Google Scholar 

  48. Lumeng CN, Bodzin JL, Saltiel AR (2007) Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 117(1):175–184. doi:10.1172/JCI29881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Kim HJ, Higashimori T, Park SY, Choi H, Dong J, Kim YJ, Noh HL, Cho YR, Cline G, Kim YB, Kim JK (2004) Differential effects of interleukin-6 and -10 on skeletal muscle and liver insulin action in vivo. Diabetes 53(4):1060–1067

    Article  CAS  PubMed  Google Scholar 

  50. Meshkani R, Adeli K (2009) Hepatic insulin resistance, metabolic syndrome and cardiovascular disease. Clin Biochem 42(13–14):1331–1346. doi:10.1016/j.clinbiochem.2009.05.018

    Article  CAS  PubMed  Google Scholar 

  51. Forstermann U, Sessa WC (2012) Nitric oxide synthases: regulation and function. Eur Heart J 33(7):829–837, 837a-837d. doi:10.1093/eurheartj/ehr304

    Article  CAS  PubMed  Google Scholar 

  52. Ricciotti E, FitzGerald GA (2011) Prostaglandins and inflammation. Arterioscler Thromb Vasc Biol 31(5):986–1000. doi:10.1161/ATVBAHA.110.207449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Fitzgerald RJ, Murray BA (2006) Bioactive peptides and lactic fermentations. Int J Dairy Technol 59(2):118–125. doi:10.1111/j.1471-0307.2006.00250.x

    Article  CAS  Google Scholar 

  54. Masuyer G, Schwager SL, Sturrock ED, Isaac RE, Acharya KR (2012) Molecular recognition and regulation of human angiotensin-I converting enzyme (ACE) activity by natural inhibitory peptides. Sci Rep 2:717. doi:10.1038/srep00717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Rutella GS, Tagliazucchi D, Solieri L (2016) Survival and bioactivities of selected probiotic lactobacilli in yogurt fermentation and cold storage: new insights for developing a bi-functional dairy food. Food Microbiol 60:54–61. doi:10.1016/j.fm.2016.06.017

    Article  CAS  PubMed  Google Scholar 

  56. Nurminen ML, Sipola M, Kaarto H, Pihlanto-Leppala A, Piilola K, Korpela R, Tossavainen O, Korhonen H, Vapaatalo H (2000) Alpha-lactorphin lowers blood pressure measured by radiotelemetry in normotensive and spontaneously hypertensive rats. Life Sci 66(16):1535–1543. doi:10.1016/S0024-3205(00)00471-9

    Article  CAS  PubMed  Google Scholar 

  57. Seppo L, Jauhiainen T, Poussa T, Korpela R (2003) A fermented milk high in bioactive peptides has a blood pressure-lowering effect in hypertensive subjects. Am J Clin Nutr 77(2):326–330

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was co-financed by the European Regional Development Fund (ERDF) of the EU and by the Greek National Resources under the Operational Program Competitiveness and Entrepreneurship (OPCE II), Action “COOPERATION 2011”, Partnerships of Production and Research Institutions in Focused Research and Technology Sectors—Project 11SYN_2_571_ProbioDairyMeat.

Author information

Authors and Affiliations

  1. Laboratory of Dairy Research, Department of Food Science and Human Nutrition, Agricultural University of Athens, Iera Odos 75, 11855, Athens, Greece

    Georgia Zoumpopoulou, Alexandra Tzouvanou, Voula Alexandraki, Marina Georgalaki, Rania Anastasiou, Marina Papadelli, Eugenia Manolopoulou, Maria Kazou, Konstantinos Papadimitriou & Effie Tsakalidou

  2. Laboratory of Cell Proliferation and Ageing, Institute of Biosciences and Applications, National Centre for Scientific Research “Demokritos”, Patr. Gregoriou E’ & Neapoleos 27, 15310, Athens, Greece

    Eleni Mavrogonatou & Dimitris Kletsas

Authors
  1. Georgia Zoumpopoulou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alexandra Tzouvanou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eleni Mavrogonatou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Voula Alexandraki
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marina Georgalaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rania Anastasiou
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marina Papadelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Eugenia Manolopoulou
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Maria Kazou
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Dimitris Kletsas
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Konstantinos Papadimitriou
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Effie Tsakalidou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Georgia Zoumpopoulou.

Ethics declarations

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of Interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

ESM 1

(PDF 171 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zoumpopoulou, G., Tzouvanou, A., Mavrogonatou, E. et al. Probiotic Features of Lactic Acid Bacteria Isolated from a Diverse Pool of Traditional Greek Dairy Products Regarding Specific Strain-Host Interactions. Probiotics & Antimicro. Prot. 10, 313–322 (2018). https://doi.org/10.1007/s12602-017-9311-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-017-9311-9

Keywords

Search

Navigation