Skip to main content

Advertisement

Log in

Characterization of Lactic Acid Bacteria in Raw Buffalo Milk: a Screening for Novel Probiotic Candidates and Their Transcriptional Response to Acid Stress

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

Abstract

Lactic acid bacteria (LAB) are important microorganisms for the food industry due to their functional activity, as starters and potential probiotic strains. With that in mind, we explored the LAB diversity in raw buffalo milk, screening for novel potential probiotic strains. A total of 11 strains were identified by combination of MALDI-TOF and partial 16S rDNA sequencing and selected as potential probiotic candidates. Bacteria innocuity assessment was performed by determining antimicrobial susceptibility and the presence of virulence factors. Antagonism activity against Escherichia coli, Pseudomonas aeruginosa, Listeria monocytogenes and Staphylococcus aureus was assessed, as well as milk proteolytic activity and exopolysaccharides production. Seven strains were identified as innocuous and two of them, Lactobacillus rhamnosus LB1.5 and Lactobacillus paracasei LB6.4 were selected for further probiotic potential analyses. Both strains demonstrated adhesion ability to Caco-2 cells, coaggregated with S. aureus and E. coli and maintained cell viability after gastrointestinal simulation in vitro, suggesting their probiotic potential. Furthermore, the transcriptional response of Lact. rhamnosus LB1.5 and Lact. paracasei LB6.4 to in vitro acid stress was assessed by RT-qPCR targeting seven genes related to adhesion, aggregation, stress tolerance, DNA repair and central metabolism. The association between the transcriptional responses and the maintenance of cell viability after gastrointestinal simulation highlights the genetic ability as probiotic of the two selected strains. Finally, we have concluded that Lact. rhamnosus LB1.5 and Lact. paracasei LB6.4 are important probiotic candidates to further in vivo studies.

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

Access this article

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

Data Availability

Not applicable.

References

  1. Yang TX, Wang F, Li H, Liu QS, Li QY (2013) The nutrition of buffalo milk: a comparison with cow milk. Adv Mater Res 781-784:1460–1463. https://doi.org/10.4028/www.scientific.net/amr.781-784.1460

    Article  Google Scholar 

  2. Food and Agriculture Organization of the United Nations/World Health Organization (2002) Guidelines for the evaluation of probiotics in food. Food and Agriculture Organization of the United Nations and World Health Organization Working Group Report. Geneva, Switzerland: World Health Organization. https://www.who.int/foodsafety/fs_management/en/probiotic_guidelines.pdf Accessed 21 April 2020

  3. Khare A, Gaur S (2020) Cholesterol-lowering effects of Lactobacillus species. Curr Microbiol 77(4):638–644. https://doi.org/10.1007/s00284-020-01903-w

    Article  CAS  PubMed  Google Scholar 

  4. Thumu SCR, Halami PM (2020) In vivo safety assessment of Lactobacillus fermentum strains, evaluation of their cholesterol-lowering ability and intestinal microbial modulation. J Sci Food Agric 100(2):705–713. https://doi.org/10.1002/jsfa.10071

    Article  CAS  PubMed  Google Scholar 

  5. Harper A, Naghibi MM, Garcha D (2018) The role of bacteria, probiotics and diet in irritable bowel syndrome. Foods 7(2):13. https://doi.org/10.3390/foods7020013

    Article  CAS  PubMed Central  Google Scholar 

  6. Niu HL, Xiao JY (2020) The efficacy and safety of probiotics in patients with irritable bowel syndrome: evidence based on 35 randomized controlled trials. Int J Surg 75:116–127. https://doi.org/10.1016/j.ijsu.2020.01.142

    Article  PubMed  Google Scholar 

  7. Santos FDS, Mazzoli A, Maia AR, Saggese A, Isticato R, Leite F, Iossa S, Ricca E, Baccigalupi L (2020) A probiotic treatment increases the immune response induced by the nasal delivery of spore-adsorbed TTFC. Microb Cell Factories 19(1):42. https://doi.org/10.1186/s12934-020-01308-1

    Article  CAS  Google Scholar 

  8. Kadooka Y, Sato M, Ogawa A, Miyoshi M, Uenishi H, Ogawa H, Ikuyama K, Kagoshima M, Tsuchida T (2013) Effect of Lactobacillus gasseri SBT2055 in fermented milk on abdominal adiposity in adults in a randomised controlled trial. Br J Nutr 110(9):1696–1703. https://doi.org/10.1017/S0007114513001037

    Article  CAS  PubMed  Google Scholar 

  9. Sharafedtinov KK, Plotnikova OA, Alexeeva RI, Sentsova TB, Songisepp E, Stsepetova J, Smidt I, Mikelsaar M (2013) Hypocaloric diet supplemented with probiotic cheese improves body mass index and blood pressure indices of obese hypertensive patients: a randomized double-blind placebo-controlled pilot study. Nutr J 12:138. https://doi.org/10.1186/1475-2891-12-138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Razmpoosh E, Zare S, Fallahsadeh H et al (2020) Effect of a low energy diet, containing a high protein, probiotic condensed yogurt, on biochemical and anthropometric measurements among women with overweight/obesity: a randomised controlled trial. Clin Nutr ESPEN 35:194–200. https://doi.org/10.1016/j.clnesp.2019.10.001

    Article  PubMed  Google Scholar 

  11. Madera C, García P, Jansen T et al (2003) Characterization of technologically proficient wild Lactococcus lactis strains resistant to phage infection. Int J Food Microbiol 86(3):213–222. https://doi.org/10.1016/S0168-1605(03)00042-4

    Article  PubMed  Google Scholar 

  12. Klein G, Pack A, Bonaparte C, Reuter G (1998) Taxonomy and physiology of probiotic lactic acid bacteria. Int J Food Microbiol 41(2):103–125. https://doi.org/10.1016/S0168-1605(98)00049-X

    Article  CAS  PubMed  Google Scholar 

  13. Vijaya Kumar B, Vijayendra SVN, Reddy OVS (2015) Trends in dairy and non-dairy probiotic products – a review. J Food Sci Technol 52(10):6112–6124. https://doi.org/10.1007/s13197-015-1795-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Kaktcham PM, Zambou NF, Tchouanguep FM, el-Soda M, Choudhary MI (2012) Antimicrobial and safety properties of Lactobacilli isolated from two Cameroonian traditional fermented foods. Sci Pharm 80(1):189–203. https://doi.org/10.3797/scipharm.1107-12

    Article  CAS  PubMed  Google Scholar 

  15. Bezkorovainy A (2001) Probiotics: determinants of survival and growth in the gut. Am J Clin Nutr 73(2 Suppl):399S–405S. https://doi.org/10.1093/ajcn/73.2.399s

    Article  CAS  PubMed  Google Scholar 

  16. Marteau P, Minekus M, Havenaar R, Huis in’t Veld HS (1997) Survival of lactic acid bacteria in a dynamic model of the stomach and small intestine: validation and the effects of bile. J Dairy Sci 80(6):1031–1037. https://doi.org/10.3168/jds.S0022-0302(97)76027-2

    Article  CAS  PubMed  Google Scholar 

  17. Papadimitriu K, Alegría A, Bron PA et al (2016) Stress physiology of lactic acid bacteria. Microbiol Mol Biol Rev 80(3):837–890. https://doi.org/10.1128/MMBR.00076-15

    Article  Google Scholar 

  18. Medeiros AW, Pereira RI, Oliveira DV, Martins PD, d’Azevedo PA, van der Sand S, Frazzon J, Frazzon APG (2014) Molecular detection of virulence factors among food and clinical Enterococcus faecalis strains in South Brazil. Braz J Microbiol 45(1):327–332. https://doi.org/10.1590/S1517-83822014005000031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Depardieu F, Perichon B, Courvalin P (2004) Detection of the van alphabet and identification of Enterococci and Staphylococci at the species level by multiplex PCR. J Clin Microbiol 42(12):5857–5860. https://doi.org/10.1128/JCM.42.12.5857-5860.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Gontang EA, Fenical W, Jensen PR (2007) Phylogenetic diversity of gram-positive bacteria cultured from marine sediments. Appl Environ Microbiol 73:3272–3282. https://doi.org/10.1128/AEM.02811-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454

    Article  CAS  PubMed  Google Scholar 

  22. Bauer AW, Kirby WMM, Sherris JC, Turck M (1966) Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 45(4):493–496

    Article  CAS  PubMed  Google Scholar 

  23. Clinical and Laboratory Standards Institute (2015) Performance standards for antimicrobial susceptibility testing; Twenty-Fifth Informational Supplement (M100-S25). Clinical and Laboratory Standards Institute, Wayne, PA

    Google Scholar 

  24. Clinical and Laboratory Standards Institute (2011) Methods for antimicrobial dilution and disk susceptibility testinf of infrequently isolated or fastidious bacteria; approved guideline - Second Edition (M45-A2). Clinical and Laboratory Standards Institute, Wayne, PA

    Google Scholar 

  25. Maragkoudakis PA, Zoumpopoulou G, Miaris C, Kalantzopoulos G, Pot B, Tsakalidou E (2006) Probiotic potential of Lactobacillus strains isolated from dairy products. Int Dairy J 16:189–199. https://doi.org/10.1016/j.idairyj.2005.02.009

    Article  CAS  Google Scholar 

  26. Marra A, Dib-Hajj F, Lamb L, Kaczmarek F, Shang W, Beckius G, Milici AJ, Medina I, Gootz TD (2007) Enterococcal virulence determinants may be involved in resistance to clinical therapy. Diagn Microbiol Infect Dis 58(1):59–65. https://doi.org/10.1016/j.diagmicrobio.2006.11.024

    Article  CAS  PubMed  Google Scholar 

  27. Souza BMS, Borgonovi TF, Casarotti SN et al (2019) Lactobacillus casei and Lactobacillus fermentum strains isolated from mozzarella cheese: probiotic potential, safety, acidifying kinetic parameters and viability under gastrointestinal tract conditions. Probiotics Antimicrob Proteins 11(2):382–396. https://doi.org/10.1007/s12602-018-9406-y

    Article  CAS  PubMed  Google Scholar 

  28. Omar NB, Castro A, Lucas R, Abriouel H, Yousif NMK, Franz CMAP, Holzapfel WH, Rubén PP, Martínez-Canãmero M, Gálvez A (2004) Functional and safety aspects of enterococci isolated from different Spanish foods. Syst Appl Microbiol 27(1):118–130. https://doi.org/10.1078/0723-2020-00248

    Article  PubMed  Google Scholar 

  29. Eaton TJ, Gasson MJ (2001) Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl Environ Microbiol 67(4):1628–1635. https://doi.org/10.1128/AEM.67.4.1628-1635.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Vankerckhoven V, Van Autgaerden T, Vael C et al (2004) Development of a multiplex PCR for the detection of asaI, gelE, cylA, esp, and hyl genes in enterococci and survey for virulence determinants among european hospital isolates of Enterococcus faecium. J Clin Microbiol 42(10):4473–4479. https://doi.org/10.1128/JCM.42.10.4473-4479.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Lopes FMS, Simões AP, Tenreiro R et al (2006) Activity and expression of a virulence factor, gelatinase, in dairy enterococci. Int J Food Microbiol 112(3):208–214. https://doi.org/10.1016/j.ijfoodmicro.2006.09.004

    Article  CAS  Google Scholar 

  32. Kapse NG, Engineer AS, Gowdaman V, Wagh S, Dhakephalkar PK (2019) Functional annotation of the genome unravels probiotic potential of Bacillus coagulans HS243. Genomics 111(4):921–929. https://doi.org/10.1016/j.ygeno.2018.05.022

    Article  CAS  PubMed  Google Scholar 

  33. Mora D, Fortina MG, Parini C, Ricci G, Gatti M, Giraffa G, Manachini PL (2002) Genetic diversity and technological properties of Streptococcus thermophilus strains isolated from dairy products. J Appl Microbiol 93(2):278–287. https://doi.org/10.1046/j.1365-2672.2002.01696.x

    Article  CAS  PubMed  Google Scholar 

  34. Stingele F, Neeser J (1996) Identification and characterization of the eps (exopolysaccharide) gene cluster from Streptococcus thermophilus Sfi6. J Bacteriol 178(6):1680–1690. https://doi.org/10.1128/jb.178.6.1680-1690.1996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Montanhini MTM, Bersot LS (2013) Evaluation of psychrotrophic behavior and lipolytic and proteolytic activity of Bacillus cereus isolated from refrigerated dairy products. Acta Sci Technol 35(1):163–174. https://doi.org/10.4025/actascitechnol.v35i1.13752

    Article  CAS  Google Scholar 

  36. Todorov SD, Dicks LMT (2008) Evaluation of lactic acid bacteria from kefir, molasses and olive brine as possible probiotics based on physiological properties. Ann Microbiol 58(4):661–670. https://doi.org/10.1007/BF03175572

    Article  Google Scholar 

  37. Del Re B, Sgorbati B, Miglioli M, Palenzona D (2000) Adhesion, autoaggregation and hydrophobicity of 13 strains of Bifidobacterium longum. Lett Appl Microbiol 31(6):438–442. https://doi.org/10.1046/j.1365-2672.2000.00845.x

    Article  PubMed  Google Scholar 

  38. Zuo F, Appaswamy A, Gebremariam HG, Jonsson AB (2019) Role of Sortase a in Lactobacillus gasseri KX110A1 adhesion to gastric epithelial cells and competitive exclusion of Helicobacter pylori. Front Microbiol 10:2770. https://doi.org/10.3389/fmicb.2019.02770

    Article  PubMed  PubMed Central  Google Scholar 

  39. Iraporda C, Rubel IA, Manrique GD, Abraham AG (2019) Influence in inulin rich carbohydrates from Jerusalem artichoke (Helianthus tuberosus L.) tubers on probiotic properties of Lactobacillus strains. LWT-Food Sci Technol 101:738–746. https://doi.org/10.1016/j.lwt.2018.11.074

    Article  CAS  Google Scholar 

  40. Fortina MG, Ricci G, Borgo F, Manachini PL, Arends K, Schiwon K, Abajy MY, Grohmann E (2008) A survey on biotechnological potential and safety of the novel Enterococcus species of dairy origin, E italicus. Int J Food Microbiol 123(3):204–211. https://doi.org/10.1016/j.ijfoodmicro.2008.01.014

    Article  CAS  PubMed  Google Scholar 

  41. Zhao H, Liu L, Peng S, Yuan L, Li H, Wang H (2019) Heterologous expression of argininosuccinate synthase from Oenococcus oeni enhances the acid resistance of Lactobacillus plantarum. Front Microbiol 10:1393. https://doi.org/10.3389/fmicb.2019.01393

    Article  PubMed  PubMed Central  Google Scholar 

  42. Livak KJ, Schimittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262

    Article  CAS  PubMed  Google Scholar 

  43. Bizzini A, Durussel C, Bille J, Greub G, Prod’hom G (2010) Performance of matrix-assisted laser desorption ionization-time of flight mass spectrometry for identification of bacterial strains routinely isolated in a clinical microbiology laboratory. J Clin Microbiol 48(5):1549–1554. https://doi.org/10.1128/JCM.01794-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Neville SA, LeCordier A, Ziochos H, Chater MJ, Gosbell IB, Maley MW, van Hal SJ (2011) Utility of matrix-assisted laser desorption ionization-time of flight mass spectrometry following introduction for routine laboratory bacterial identification. J Clin Microbiol 49(8):2980–2984. https://doi.org/10.1128/JCM.00431-11

    Article  PubMed  PubMed Central  Google Scholar 

  45. Torriani S, Clementi F, Vancanneyt M, Hoste B, Dellaglio F, Kersters K (2001) Differentiation of Lactobacillus plantarum, L. pentosus and L. paraplantarum species by RAPD-PCR and AFLP. Syst Appl Microbiol 24(4):554–560. https://doi.org/10.1078/0723-2020-00071

    Article  CAS  PubMed  Google Scholar 

  46. Huang CH, Lee FL, Liou JS (2010) Rapid discrimination and classification of the Lactobacillus plantarum group based on a partial dnaK sequence and DNA fingerprinting techniques. Antonie Van Leeuwenhoek 97(3):289–296. https://doi.org/10.1007/s10482-009-9409-5

    Article  CAS  PubMed  Google Scholar 

  47. Huang CH, Lee FL (2011) The dnaK gene as a molecular marker for the classification and discrimination of the Lactobacillus casei group. Antonie Van Leeuwenhoek 99(2):319–327. https://doi.org/10.1007/s10482-010-9493-6

    Article  PubMed  Google Scholar 

  48. Angelakis E, Million M, Henry M, Raoult D (2011) Rapid and accurate bacterial identification in probiotics and yoghurts by MALDI-TOF mass spectrometry. J Food Sci 76(8):M568–M572. https://doi.org/10.1111/j.1750-3841.2011.02369.x

    Article  CAS  PubMed  Google Scholar 

  49. Doan NTL, Van Hoorde K, Cnockaert M et al (2012) Validation of MALDI-TOF MS for rapid classification and identification of lactic acid bacteria, with a focus on isolates from traditional fermented foods in Northern Vietnam. Lett Appl Microbiol 55(4):265–273. https://doi.org/10.1111/j.1472-765X.2012.03287.x

    Article  CAS  PubMed  Google Scholar 

  50. Nacef M, Chevalier M, Chollet S, Drider D, Flahaut C (2017) MALDITOF mass spectrometry for the identification of lactic acid bacteria isolated from a French cheese: the Maroilles. Int J Food Microbiol 247:2–8. https://doi.org/10.1016/j.ijfoodmicro.2016.07.005

    Article  CAS  PubMed  Google Scholar 

  51. Lee Y, Cho Y, Kim E, Kim HJ, Kim HY (2018) Identification of lactic acid bacteria in Galchi- and Myeolchi-Jeotgal by 16S rRNA gene sequencing, MALDI-TOF mass spectrometry, and PCR-DGGE. J Microbiol Biotechnol 28(7):1112–1121. https://doi.org/10.4014/jmb.1803.03034

    Article  CAS  PubMed  Google Scholar 

  52. Ansari JM, Colasacco C, Emmanouil E, Kohlhepp S, Harriott O (2019) Strain-level diversity of commercial probiotic isolates of Bacillus, Lactobacillus, and Saccharomyces species illustrated by molecular identification and phenotypic profiling. PLoS One 14(3):e0213841. https://doi.org/10.1371/journal.pone.0213841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Meira SMM, Helfer VE, Velho RV, Lopes FC (2012) Probiotic potential of Lactobacillus spp. isolated from Brazilian regional ovine cheese. J Dairy Res 79(1):119–127. https://doi.org/10.1017/S0022029911000884

    Article  CAS  PubMed  Google Scholar 

  54. Gaglio R, Couto N, Marques C, de Fatima Silva Lopes M, Moschetti G, Pomba C, Settanni L (2016) Evaluation of antimicrobial resistance and virulence of enterococci from equipment surfaces, raw materials, and traditional cheeses. Int J Food Microbiol 236:107–114. https://doi.org/10.1016/j.ijfoodmicro.2016.07.020

    Article  CAS  PubMed  Google Scholar 

  55. Zhou JS, Shu Q, Rutherfurd KJ, Prasad J, Birtles MJ, Gopal PK, Gill HS (2000) Safety assessment of potential probiotic lactic acid bacterial strains Lactobacillus rhamnosus HN001, Lb. acidophilus HN017, and Bifidobacterium lactis HN019 in BALB/c mice. Int J Food Microbiol 56(1):87–96. https://doi.org/10.1016/S0168-1605(00)00219-1

    Article  CAS  PubMed  Google Scholar 

  56. Harwood VJ, Brownell M, Perusek W, Whitlock JE (2001) Vancomycin-resistant Enterococcus spp. isolated from wastewater and chicken feces in the United States. Appl Environ Microbiol 67(10):4930–4933. https://doi.org/10.1128/AEM.67.10.4930-4933.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Halami PM, Chandrashekar A, Nand K (2000) Lactobacillus farciminis MD, a newer strain with potential for bacteriocin and antibiotic assay. Lett Appl Microbiol 30(3):197–202. https://doi.org/10.1046/j.1472-765x.2000.00691.x

    Article  CAS  PubMed  Google Scholar 

  58. Anisimova EA, Yarullina DR (2019) Antibiotic resistance of Lactobacillus strains. Curr Microbiol 76(12):1407–1416. https://doi.org/10.1007/s00284-019-01769-7

    Article  CAS  PubMed  Google Scholar 

  59. Kaboré WAD, Dembélé R, Bagré TS, Konaté A, Boisramé S, Chevalier V, Konsem T, Traoré A, Barro N (2018) Characterization and antimicrobial susceptibility of Lactococcus lactis isolated from endodontic infections in Ouagadougou, Burkina Faso. Dent J 6(4):69. https://doi.org/10.3390/dj6040069

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  61. Todorov SD, Botes M, Danova ST, Dicks LMT (2007) Probiotic properties of Lactococcus lactis ssp. lactis HV219, isolated from human vaginal secretions. J Appl Microbiol 103(3):629–639. https://doi.org/10.1111/j.1365-2672.2007.03290.x

    Article  CAS  PubMed  Google Scholar 

  62. Todorov SD, Franco BDGM (2018) In vitro study of some safety and beneficial properties of bacteriocinogenic Lactococcus lactis subsp. lactis MK02R. Chem Eng Trans 64:133–138 https://www.aidic.it/cet/18/64/023.pdf Accessed 22 July 2020

    Google Scholar 

  63. Yerlikaya O (2019) Probiotic potential and biochemical and technological properties of Lactococcus lactis ssp. lactis strains isolated from raw milk and kefir grains. J Dairy Sci 102(1):124–134. https://doi.org/10.3168/jds.2018-14983

    Article  CAS  PubMed  Google Scholar 

  64. Teuber M, Meile L, Schwarz F (1999) Acquired antibiotic resistance in lactic acid bacteria from food. Antonie Van Leeuwenhoek 76(1–4):115–137. https://doi.org/10.1023/A:1002035622988

    Article  CAS  PubMed  Google Scholar 

  65. Gevers D, Danielsen M, Huys G, Swings J (2003) Molecular characterization of tet(M) genes in Lactobacillus isolates from different types of fermented dry sausage. Appl Environ Microbiol 69(2):1270–1275. https://doi.org/10.1128/AEM.69.2.1270-1275.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Alexandre DP, Silva MR, Souza MR et al (2002) Antimicrobial activity of lactic acid bacteria from artisanal and “coalho” cheese against indicator microorganisms. Arq Bras Med Vet Zootec 57(Suppl 2):245–250 https://www.scielo.br/pdf/abmvz/v57s2/28329.pdf Accessed 22 July 2020

    Google Scholar 

  67. Campagnollo FB, Margalho LP, Kamimura BA, Feliciano MD, Freire L, Lopes LS, Alvarenga VO, Cadavez VAP, Gonzales-Barron U, Schaffner DW, Sant’Ana AS (2018) Selection of indigenous lactic acid bacteria presenting anti-listerial activity, and their role in reducing the maturation period and assuring the safety of traditional Brazilian cheeses. Food Microbiol 73:288–297. https://doi.org/10.1016/j.fm.2018.02.006

    Article  CAS  PubMed  Google Scholar 

  68. Ortolani MBT, Moraes PM, Perin LM, Viçosa GN, Carvalho KG, Silva Júnior A, Nero LA (2010) Molecular identification of naturally occurring bacteriocinogenic and bacteriocinogenic-like lactic acid bacteria in raw milk and soft cheese. J Dairy Sci 93(7):2880–2886. https://doi.org/10.3168/jds.2009-3000

    Article  CAS  PubMed  Google Scholar 

  69. Adebayo-Tayo B, Fushogbon R (2020) In vitro antioxidant, antibacterial, in vivo immunomodulatory, antitumor and haematological potential of exopolysaccharide produced by wild type and mutant Lactobacillus delbureckii subsp. bulgaricus. Heliyon 6(2):e03268. https://doi.org/10.1016/j.heliyon.2020.e03268

    Article  PubMed  PubMed Central  Google Scholar 

  70. Nagaoka M, Hashimoto S, Watanabe T et al (1994) Anti-ulcer effects of lactic acid bacteria and their cell wall polysaccharides. Biol Pharm Bull 17(8):1012–1017. https://doi.org/10.1248/bpb.17.1012

    Article  CAS  PubMed  Google Scholar 

  71. Sasikumar K, Kozhummal VD, Devendra L, Nampoothiri KM (2017) An exopolysaccharide (EPS) from a Lactobacillus plantarum BR2 with potential benefits for making functional foods. Bioresour Technol 241:1152–1156. https://doi.org/10.1016/j.biortech.2017.05.075

    Article  CAS  PubMed  Google Scholar 

  72. Ispirli H, Demirbas F, Dertli E (2018) Glucan type exopolysaccharide (EPS) shows prebiotic effect and reduces syneresis in chocolate pudding. J Food Sci Technol 55(9):3821–3826. https://doi.org/10.1007/s13197-018-3181-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Mahdhi A, Leban N, Chakroun I, Chaouch MA, Hafsa J, Fdhila K, Mahdouani K, Majdoub H (2017) Extracellular polysaccharide derived from potential probiotic strain with antioxidant and antibacterial activities as a prebiotic agent to control pathogenic bacterial biofilm formation. Microb Pathog 109:214–220. https://doi.org/10.1016/j.micpath.2017.05.046

    Article  CAS  PubMed  Google Scholar 

  74. Albenzio M, Santillo A, Caroprese M, Marino R, Trani A, Faccia M (2010) Biochemical patterns in ovine cheese: influence of probiotic strains. J Dairy Sci 93(8):3487–3496. https://doi.org/10.3168/jds.2009-3036

    Article  CAS  PubMed  Google Scholar 

  75. Tuomola EM, Ouwehand AC, Salminen SJ (2000) Chemical, physical and enzymatic pre-treatments of probiotic lactobacilli alter their adhesion to human intestinal mucus glycoproteins. Int J Food Microbiol 60(1):75–81. https://doi.org/10.1016/s0168-1605(00)00319-6

    Article  CAS  PubMed  Google Scholar 

  76. Ayala DI, Cook PW, Franco JG, Bugarel M, Kottapalli KR, Loneragan GH, Brashears MM, Nightingale KK (2019) A systematic approach to identify and characterize the effectiveness and safety of novel probiotic strains to control foodborne pathogens. Front Microbiol 10:1108. https://doi.org/10.3389/fmicb.2019.01108

    Article  PubMed  PubMed Central  Google Scholar 

  77. Chondrou P, Karapetsas A, Kiousi DE, Vasileiadis S, Ypsilantis P, Botaitis S, Alexopoulos A, Plessas S, Bezirtzoglou E, Galanis A (2020) Assessment of the immunomodulatory properties of the probiotic strain Lactobacillus paracasei K5 in vitro and in vivo. Microorganisms 8(5):709. https://doi.org/10.3390/microorganisms8050709

    Article  CAS  PubMed Central  Google Scholar 

  78. Salehizadeh M, Modarressi MH, Mousavi SN, Tajabadi Ebrahimi M (2020) Evaluation of lactic acid bacteria isolated from poultry feces as potential probiotic and its in vitro competitive activity against Salmonella typhimurium. Vet Res Forum 11(1):67–75. https://doi.org/10.30466/vrf.2018.84395.2110

    Article  PubMed  PubMed Central  Google Scholar 

  79. Engle MJ, Goetz GS, Alpers DH (1998) Caco-2 cells express a combination of colonocyte and enterocyte phenotypes. J Cell Physiol 174(3):362–369. https://doi.org/10.1002/(SICI)1097-4652(199803)174:3<362::AID-JCP10>3.0.CO;2-B

    Article  CAS  PubMed  Google Scholar 

  80. García-Ruiz A, González LD, Esteban-Fernández A et al (2014) Assessment of probiotic properties in lactic acid bacteria isolated from wine. Food Microbiol 44:220–225. https://doi.org/10.1016/j.fm.2014.06.015

    Article  CAS  PubMed  Google Scholar 

  81. Arellano K, Vazquez J, Park H, Lim J, Ji Y, Kang HJ, Cho D, Jeong HW, Holzapfel WH (2019) Safety evaluation and whole-genome annotation of Lactobacillus plantarum strains from different sources with special focus on isolated from green tea. Probiotics Antimicrob Proteins Advance online publication. https://doi.org/10.1007/s12602-019-09620-y

  82. Kos B, Suskovic JS, Vukovic S et al (2003) Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J Appl Microbiol 94(6):981–987. https://doi.org/10.1046/j.1365-2672.2003.01915.x

    Article  CAS  PubMed  Google Scholar 

  83. Le B, Yang SH (2019) Identification of a novel potential probiotic Lactobacillus plantarum FB003 isolated from salted-fermented shrimp and its effect on cholesterol absorption by regulation of NPC1L1 and PPARα. Probiotics Antimicrob Proteins 11(3):785–793. https://doi.org/10.1007/s12602-018-9469-9

    Article  CAS  PubMed  Google Scholar 

  84. Wu C, Zhang J, Du G, Chen J (2013) Aspartate protects Lactobacillus casei against acid stress. Appl Microbiol Biotechnol 97(9):4083–4093. https://doi.org/10.1007/s00253-012-4647-2

    Article  CAS  PubMed  Google Scholar 

  85. Zhang J, Wu C, Du G, Chen J (2012) Enhanced acid tolerance in Lactobacillus casei by adaptive evolution and compared stress response during acid stress. Biotechnol Bioproc 17:283–289. https://doi.org/10.1007/s12257-011-0346-6

    Article  CAS  Google Scholar 

  86. Wu C, Zhang J, Wang M, du G, Chen J (2012) Lactobacillus casei combats acid stress by maintaining cell membrane functionality. J Ind Microbiol Biotechnol 39(7):1031–1039. https://doi.org/10.1007/s10295-012-1104-2

    Article  CAS  PubMed  Google Scholar 

  87. Wu R, Zhang WY, Sun T, Wu J, Yue X, Meng H, Zhang H (2011) Proteomic analysis of responses of a new probiotic bacterium Lactobacillus casei Zhang to low acid stress. Int J Food Microbiol 147(3):181–187. https://doi.org/10.1016/j.ijfoodmicro.2011.04.003

    Article  CAS  PubMed  Google Scholar 

  88. Watanabe M, Kinoshita H, Nitta M, Yukishita R, Kawai Y, Kimura K, Taketomo N, Yamazaki Y, Tateno Y, Miura K, Horii A, Kitazawa H, Saito T (2010) Identification of a new adhesin-like protein from Lactobacillus mucosae ME-340 with specific affinity to the human blood group A and B antigens. J Appl Microbiol 109(3):927–935. https://doi.org/10.1111/j.1365-2672.2010.04719.x

    Article  CAS  PubMed  Google Scholar 

  89. Kvint K, Nachin L, Diez A, Nyström T (2003) The bacterial universal stress protein: function and regulation. Curr Opin Microbiol 6(2):140–145. https://doi.org/10.1016/S1369-5274(03)00025-0

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors acknowledge Cooperbúfalo, RS, for supporting our research and all collections and the Virology Laboratory of the Veterinary Faculty of UFRGS for the assistance with adherence analysis.

Code Availability

Not applicable.

Funding

This research was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Amanda de Souza da Motta.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

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

Electronic Supplementary Material

ESM 1

(XLSX 18 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Breyer, G.M., Arechavaleta, N.N., Siqueira, F.M. et al. Characterization of Lactic Acid Bacteria in Raw Buffalo Milk: a Screening for Novel Probiotic Candidates and Their Transcriptional Response to Acid Stress. Probiotics & Antimicro. Prot. 13, 468–483 (2021). https://doi.org/10.1007/s12602-020-09700-4

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-020-09700-4

Keywords

Navigation