Cited by 88Probiotics and Fermented FoodsReproductive tract infections researchAquaculture disease management and microbiota

Gastrointestinal transit tolerance, cell surface hydrophobicity, and functional attributes of Lactobacillus Acidophilus strains isolated from Indigenous Dahi

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Farid, Wajiha, Masud, Tariq, Sohail, Asma, Ahmad, Nazir, Naqvi, S. M. Saqlan, Khan, Sipper, Ali, Amjad, Khalifa, Salah A. +5 more·2021·Food Science & Nutrition

Abstract

Strains of Lactobacillus acidophilus WFA1 (KU877440), WFA2 (KU877441), and WFA3 (KU877442) were isolated from indigenous Dahi (yogurt), screened, and selected based on acid and bile tolerance along with the antimicrobial activity. These selected strains were further assessed for their probiotic and functional attributes. Results for simulated gastric and intestinal tolerance/ resistance revealed that all three strains can resist and survive under the following mentioned conditions. To access cell surface hydrophobicity, bacterial adhesion to hydrocarbons (BATH), cellular auto‐aggregation, and salt aggregation were performed. In BATH, adhesion of strains against three hydrocarbons namely xylene, dichloromethane, and hexadecane was conducted. The results show that strains showed the least adhesion to xylene (54.25%) as compared to dichloromethane (55.25%) and hexadecane (56.65%). WFA1 showed maximum adherence percentage (55.48%) followed WFA2 (55.48%) and WFA3 (51.38%). Cellular auto‐aggregation varied from 21.72% to 30.73% for WFA3 and WFA1, respectively. In the salt aggregation test (SAT), WFA1, WFA2, and WFA3 aggregated at 0.6, 1.0, and 2.0 molar concentrations of ammonium sulfate, respectively. PCR amplification of bile salt hydrolase gene (bsh) was performed and sequences were submitted to the public database of NCBI and Gene bank under accession numbers, KY689139, KY689140, and KY689141. Additionally, a cholesterol‐lowering assay was conducted and up to 26% reduction in cholesterol was observed by the strains. Regarding functional properties, exopolysaccharide (EPS) production, and antioxidant potential, strain WFA1 showed promising results EPS (1.027mg/ml), DPPH (80.66%), ABTS (81.97%), and reducing power (1.787). It can be concluded from the present study that the mentioned strains of L. acidophilus (WFA1, WFA2, and WFA3) are strongly hydrophobic; thus having an ability to survive and colonize under the gastrointestinal tract which confirms their probiotic nature. Regarding their functional properties, L. acidophilus WFA1 (KU877440) showed excellent properties of antioxidants and EPS production.

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References 52 · Cited by 88

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  1. Afify, A.‐ E.‐M.‐ M., Romeilah, R. M., Sultan, S. I., & Hussein, M. M. (2012). Antioxidant activity and biological evaluations of probiotic bacteria strains. International Journal of Academic Research, 4(6), 131– 139.
  2. Arora, D. S., & Chandra, P. (2010). Assay of antioxidant potential of two Aspergillus isolates by different methods under various physio‐chemical conditions. Brazilian Journal of Microbiology, 41(3), 765– 777. 10.1590/S1517-83822010000300029 24031554 PMC3768632 · DOI
  3. Behbahani, B. A., Noshad, M., & Falah, F. (2019). Inhibition of Escherichia coli adhesion to human intestinal Caco‐2 cells by probiotic candidate Lactobacillus plantarum strain L15. Microbial Pathogenesis, 136, 103677. 31437574
  4. Chaffanel, F., Charron‐Bourgoin, F., Soligot, C., Kebouchi, M., Bertin, S., Payot, S., Le Roux, Y., & Leblond‐Bourget, N. (2018). Surface proteins involved in the adhesion of Streptococcus salivarius to human intestinal epithelial cells. Applied Microbiology and Biotechnology, 102(6), 2851– 2865. 10.1007/s00253-018-8794-y 29442170 PMC5847202 · DOI
  5. de Souza, B. M. S., Borgonovi, T. F., Casarotti, S. N., Todorov, S. D., & Penna, A. L. B. (2019). Lactobacillus casei and Lactobacillus fermentum strains isolated from mozzarella cheese: Probiotic potential, safety, acidifying kinetic parameters and viability under gastrointestinal tract conditions. Probiotics and Antimicrobial Proteins, 11(2), 382– 396. 10.1007/s12602-018-9406-y 29542032 · DOI · Paper page
  6. de Vries, M. C., Vaughan, E. E., Kleerebezem, M., & de Vos, W. M. (2006). Lactobacillus plantarum—Survival, functional and potential probiotic properties in the human intestinal tract. International Dairy Journal, 16(9), 1018– 1028. 10.1016/j.idairyj.2005.09.003 · DOI
  7. Deepak, V. Ram Kumar Pandian, S., Sivasubramaniam, S. D., Nellaiah, H., & Sundar, K. (2016). Optimization of anticancer exopolysaccharide production from probiotic Lactobacillus acidophilus by response surface methodology. Preparative Biochemistry and Biotechnology, 46(3), 288– 297. 25831127
  8. Deepak, V., Ramachandran, S., Balahmar, R. M., Pandian, S. R. K., Sivasubramaniam, S. D., Nellaiah, H., & Sundar, K. (2016). In vitro evaluation of anticancer properties of exopolysaccharides from Lactobacillus acidophilus in colon cancer cell lines. Vitro Cellular & Developmental Biology‐Animal, 52(2), 163– 173. 10.1007/s11626-015-9970-3 26659393 · DOI
  9. Farid, W., Masud, T., Sohail, A., Naqvi, S., & Qazalbash, M. A. (2016). Molecular characterization and 16S rRNA sequence analysis of probiotic lactobacillus acidophilus isolated from indigenous Dahi (Yoghurt). International Journal of Bioscience, 9(5), 19– 27.
  10. Feldmane, J., Semjonovs, P., & Ciprovica, I. (2013). Potential of exopolysaccharides in yoghurt production. International Journal of Nutrition and Food Engineering, 7(8), 767– 770.
  11. Gao, J. (2012). Antioxidant activity of Lacbacillus rhamnosus strains. M. Sc. Thesis, China.
  12. Gilliland, S., Nelson, C., & Maxwell, C. (1985). Assimilation of cholesterol by Lactobacillus acidophilus. Applied and Environmental Microbiology, 49(2), 377– 381. 10.1128/aem.49.2.377-381.1985 3920964 PMC238411 · DOI
  13. Hill, C., Guarner, F., Reid, G., Gibson, G. R., Merenstein, D. J., Pot, B., Morelli, L., Canani, R. B., Flint, H. J., Salminen, S., Calder, P. C., & Sanders, M. E. (2014). The International scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nature Reviews Gastroenterology & Hepatology, 11(8), 506– 514. 10.1038/nrgastro.2014.66 24912386 · DOI
  14. Huang, C.‐H., Ho, C.‐Y., Chen, C.‐T., Hsu, H.‐F., & Lin, Y.‐H. (2019). Probiotic BSH activity and anti‐obesity potential of Lactobacillus plantarum strain TCI378 isolated from Korean Kimchi. Preventive Nutrition and Food Science, 24(4), 434– 441. 10.3746/pnf.2019.24.4.434 31915639 PMC6941724 · DOI
  15. Ishimwe, N., Daliri, E. B., Lee, B. H., Fang, F., & Du, G. (2015). The perspective on cholesterol‐lowering mechanisms of probiotics. Molecular Nutrition & Food Research, 59(1), 94– 105. 10.1002/mnfr.201400548 25403164 · DOI
  16. Jones, M. L., Chen, H., Ouyang, W., Metz, T., & Prakash, S. (2004). Microencapsulated genetically engineered Lactobacillus plantarum 80 (pCBH1) for bile acid deconjugation and its implication in lowering cholesterol. Journal of Biomedicine and Biotechnology, 2004(1), 61– 69. 15123889 PMC545656
  17. Jose, N. M., Bunt, C. R., & Hussain, M. A. (2015). Comparison of microbiological and probiotic characteristics of lactobacilli isolates from dairy food products and animal rumen contents. Microorganisms, 3(2), 198– 212. 10.3390/microorganisms3020198 27682086 PMC5023236 · DOI
  18. Kaushik, J. K., Kumar, A., Duary, R. K., Mohanty, A. K., Grover, S., & Batish, V. K. (2009). Functional and probiotic attributes of an indigenous isolate of Lactobacillus plantarum. PLoS One, 4(12), e8099. 10.1371/journal.pone.0008099 19956615 PMC2779496 · DOI
  19. Khaleghi, M., Kermanshahi, R. K., Yaghoobi, M. M., Zarkesh‐Esfahani, S., & Baghizadeh, A. (2010). Assessment of bile salt effects on S‐layer production, slp gene expression and some physicochemical properties of Lactobacillus acidophilus ATCC 4356. Journal of Microbiology and Biotechnology, 20(4), 749– 756. 20467248
  20. Kumar, M., Nagpal, R., Kumar, R., Hemalatha, R., Verma, V., Kumar, A., Chakraborty, C., Singh, B., Marotta, F., Jain, S., & Yadav, H. (2012). Cholesterol‐lowering probiotics as potential biotherapeutics for metabolic diseases. Experimental Diabetes Research, 2012, 1– 14. 10.1155/2012/902917 PMC3352670 22611376 · DOI
  21. Liang, T.‐W., Tseng, S.‐C., & Wang, S.‐L. (2016). Production and characterization of antioxidant properties of exopolysaccharide (s) from Peanibacillus mucilaginosus TKU032. Marine Drugs, 14(2), 40. 10.3390/md14020040 PMC4771993 26907304 · DOI
  22. Lim, H.‐J., Kim, S.‐Y., & Lee, W.‐K. (2004). Isolation of cholesterol‐lowering lactic acid bacteria from human intestine for probiotic use. Journal of Veterinary Science, 5(4), 391– 395. 10.4142/jvs.2004.5.4.391 15613825 · DOI · Paper page
  23. Liu, X., Liu, W., Zhang, Q., Tian, F., Wang, G., Zhang, H., & Chen, W. (2013). Screening of lactobacilli with antagonistic activity against enteroinvasive Escherichia coli. Food Control, 30(2), 563– 568. 10.1016/j.foodcont.2012.09.002 · DOI
  24. Lye, H.‐S., Rahmat‐Ali, G. R., & Liong, M.‐T. (2010). Mechanisms of cholesterol removal by lactobacilli under conditions that mimic the human gastrointestinal tract. International Dairy Journal, 20(3), 169– 175. 10.1016/j.idairyj.2009.10.003 · DOI
  25. Nwanyanwu, C., & Abu, G. (2013). Influence of growth media on hydrophobicity of phenol‐utilizing bacteria found in petroleum refinery effluent. International Research Journal of Biological Sciences, 2, 6– 11.
  26. Oh, Y. J., & Jung, D. S. (2015). Evaluation of probiotic properties of Lactobacillus and Pediococcus strains isolated from Omegisool, a traditionally fermented millet alcoholic beverage in Korea. LWT‐Food Science and Technology, 63(1), 437– 444.
  27. Öner, Ö., Aslim, B., & Aydaş, S. B. (2014). Mechanisms of cholesterol‐lowering effects of lactobacilli and bifidobacteria strains as potential probiotics with their bsh gene analysis. Journal of Molecular Microbiology and Biotechnology, 24(1), 12– 18. 24158048
  28. Pan, M., Kumaree, K. K., & Shah, N. P. (2017). Physiological changes of surface membrane in Lactobacillus with prebiotics. Journal of Food Science, 82(3), 744– 750. 28199749
  29. Patel, A. K., Singhania, R. R., Pandey, A., & Chincholkar, S. B. (2010). Probiotic bile salt hydrolase: Current developments and perspectives. Applied Biochemistry and Biotechnology, 162(1), 166– 180. 10.1007/s12010-009-8738-1 19669939 · DOI
  30. Pereira, D. I., McCartney, A. L., & Gibson, G. R. (2003). An in vitro study of the probiotic potential of a bile‐salt‐hydrolyzing Lactobacillus fermentum strain, and determination of its cholesterol‐lowering properties. Applied and Environmental Microbiology, 69(8), 4743– 4752. 12902267 PMC169108
  31. Pisano, M. B., Viale, S., Conti, S., Fadda, M. E., Deplano, M., Melis, M. P., Deiana, M., & Cosentino, S. (2014). Preliminary evaluation of probiotic properties of Lactobacillus strains isolated from Sardinian dairy products. BioMed Research International, 2014, 286390. 25054135 PMC4099116
  32. Plourde‐Owobi, L., Seguin, D., Baudin, M.‐A., Moste, C., & Rokbi, B. (2005). Molecular characterization of Clostridium tetani strains by pulsed‐field gel electrophoresis and colony PCR. Applied and Environmental Microbiology, 71(9), 5604– 5606. 16151158 PMC1214643
  33. Polak‐Berecka, M., Waśko, A., & Kubik‐Komar, A. (2014). Optimization of culture conditions for exopolysaccharide production by a probiotic strain of Lactobacillus rhamnosus E/N. Polish Journal of Microbiology, 63(2), 253– 257. 10.33073/pjm-2014-034 25115122 · DOI
  34. Ramasamy, K., Abdullah, N., Wong, M. C., Karuthan, C., & Ho, Y. W. (2010). Bile salt deconjugation and cholesterol removal from media by Lactobacillus strains used as probiotics in chickens. Journal of the Science of Food and Agriculture, 90(1), 65– 69. 20355013
  35. Rudel, L. L., & Morris, M. (1973). Determination of cholesterol using o‐phthalaldehyde. Journal of Lipid Research, 14(3), 364– 366. 10.1016/S0022-2275(20)36896-6 14580182 · DOI
  36. Rühmann, B., Schmid, J., & Sieber, V. (2015). High throughput exopolysaccharide screening platform: From strain cultivation to monosaccharide composition and carbohydrate fingerprinting in one day. Carbohydrate Polymers, 122, 212– 220. 10.1016/j.carbpol.2014.12.021 25817661 · DOI
  37. Sahadeva, R., Leong, S., Chua, K., Tan, C., Chan, H., Tong, E., Wong, S., & Chan, H. (2011). Survival of commercial probiotic strains to pH and bile. International Food Research Journal, 18(4), 1515– 1522.
  38. Saito, K., Tomita, S., & Nakamura, T. (2019). Aggregation of Lactobacillus brevis associated with decrease in pH by glucose fermentation. Bioscience, Biotechnology, and Biochemistry, 83(8), 1523– 1529. 30822234
  39. Schillinger, U., Guigas, C., & Holzapfel, W. H. (2005). In vitro adherence and other properties of lactobacilli used in probiotic yoghurt‐like products. International Dairy Journal, 15(12), 1289– 1297.
  40. Sirilun, S., Chaiyasut, C., Kantachote, D., & Luxananil, P. (2010). Characterisation of non human origin probiotic Lactobacillus plantarum with cholesterol‐lowering property. African Journal of Microbiology Research, 4(10), 994– 1000.
  41. Soomro, A. H., & Masud, T. (2012). Probiotic characteristics of Lactobacillus spp. isolated from fermented milk product dahi. Food Science and Technology Research, 18(1), 91– 98.
  42. Suresh Kumar, A., Mody, K., & Jha, B. (2007). Bacterial exopolysaccharides–A perception. Journal of Basic Microbiology, 47(2), 103– 117. 10.1002/jobm.200610203 17440912 · DOI
  43. Tahri, K., Grill, J. P., & Schneider, F. (1997). Involvement of trihydroxyconjugated bile salts in cholesterol assimilation by bifidobacteria. Current Microbiology, 34(2), 79– 84. 10.1007/s002849900148 9003583 · DOI
  44. Tsai, C.‐C., Lin, P.‐P., Hsieh, Y.‐M., Zhang, Z.‐Y., Wu, H.‐C., & Huang, C.‐C. (2014). Cholesterol‐lowering potentials of lactic acid bacteria based on bile‐salt hydrolase activity and effect of potent strains on cholesterol metabolism in vitro and in vivo. The Scientific World Journal, 2014, 690752. 25538960 PMC4235975
  45. Tyfa, A., Kunicka‐Styczyńska, A., & Zabielska, J. (2015). Evaluation of hydrophobicity and quantitative analysis of biofilm formation by Alicyclobacillus sp. Acta Biochimica Polonica, 62(4), 785– 790. 10.18388/abp.2015_1133 26629793 · DOI
  46. Xing, J., Wang, G., Zhang, Q., Liu, X., Gu, Z., Zhang, H., Chen, Y. Q., & Chen, W. (2015). Determining antioxidant activities of lactobacilli cell‐free supernatants by cellular antioxidant assay: A comparison with traditional methods. PLoS One, 10(3), e0119058. 10.1371/journal.pone.0119058 25789875 PMC4366247 · DOI
  47. Yi, Z.‐J., Fu, Y.‐R., Li, M., Gao, K.‐S., & Zhang, X.‐G. (2009). Effect of LTA isolated from bifidobacteria on D‐galactose‐induced aging. Experimental Gerontology, 44(12), 760– 765. 10.1016/j.exger.2009.08.011 19735715 · DOI
  48. Zhou, X.‐X., Pan, Y.‐J., Wang, Y.‐B., & Li, W.‐F. (2007). In vitro assessment of gastrointestinal viability of two photosynthetic bacteria, Rhodopseudomonas palustris and Rhodobacter sphaeroides. Journal of Zhejiang University Science B, 8(9), 686– 692. 17726751 PMC1963436
  49. Zuo, F., Yu, R., Feng, X., Chen, L., Zeng, Z., Khaskheli, G. B., Ma, H., & Chen, S. (2016). Characterization and in vitro properties of potential probiotic Bifidobacterium strains isolated from breast‐fed infant feces. Annals of Microbiology, 66(3), 1027– 1037. 10.1007/s13213-015-1187-x · DOI

Authors
Farid, W., Masud, T., Sohail, A., Ahmad, N., Naqvi, S. M. S., Khan, S., Ali, A., Khalifa, S. A., Hussain, A., Ali, S., Saghir, M., Siddeeg, A., & Manzoor, M. F.
Affiliations
  • Pir Mehr Ali Shah Arid Agriculture University (PK)
  • Government College University, Faisalabad (PK)
  • University of Hohenheim (DE)
  • Karakoram International University (PK)
  • Zagazig University (EG)
  • National University of Sciences and Technology (PK)
  • University of Gezira (SD)
  • Jiangsu University (CN)
Corresponding author
  • Masud, Tariq
  • Siddeeg, Azhari
  • Manzoor, Muhammad Faisal
Venue
Food Science & Nutrition
Publisher
Wiley
Published
2021-07-13
Volume
9
Issue
9
Pages
5092-5102
ISSN
2048-7177 (ISSN-L)
OpenAlex
W3182121705
Cited by
88
References
52
Citations by year
2026: 24 · 2025: 26 · 2024: 25 · 2023: 5 · 2022: 6 · 2021: 2
FWCI
5.68
Type
journal article
Language
en
Open access
Locations
  • Food Science & Nutrition (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Higher Education Commision, Pakistan
Topics
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
  • Life Sciences › Immunology and Microbiology › Microbiology › Reproductive tract infections research
  • Life Sciences › Immunology and Microbiology › Immunology › Aquaculture disease management and microbiota
Keywords
Lactobacillus acidophilus, probiotic strains, bile tolerance, acid resistance, cell surface hydrophobicity, bile salt hydrolase, cholesterol lowering, exopolysaccharide production, antioxidant activity, antimicrobial activity, self-aggregation

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