<i>In Vitro</i> Characterization of Cell Surface Properties of 14 Vaginal <i>Lactobacillus</i> Strains as Potential Probiotics — Oak Academic Publishing
Research ArticleOpen AccessGoogle Scholar indexed
<i>In Vitro</i> Characterization of Cell Surface Properties of 14 Vaginal <i>Lactobacillus</i> Strains as Potential Probiotics
SignalDT Biotechnologies (SZ), Inc., Shenzhen, China
,
Department of Biological Engineering, Inha University, Incheon, Korea
1 SignalDT Biotechnologies (SZ), Inc., Shenzhen, China
2 Department of Biological Engineering, Inha University, Incheon, Korea
Probiotics are live microorganisms which when administered in adequate amounts confer a health benefit on the host. Human-origin Lactobacillus is a preferable source of probiotic bacteria. This study screened 14 vaginal Lactobacillus strains as probiotic candidates by investigating probiotic-related cell surface characteristics including cell surface hydrophobicity (CSH), Lewis acidity/basicity, autoaggregation, and biofilm formation. Moderate to high CSH and autoaggregation, high basicity and low acidity were prevalent in the 14 tested strains. Biofilm formation varied in a large range among the 14 tested strains. CSH showed a high correlation with Lewis acidity and autoaggregation, while Lewis acidity was highly correlated with autoaggregation and biofilm formation. Four strains were selected as promising probiotic strains. This study was the first one to compare antibiotic sensitivity between biofilm-forming cells and planktonic cells of Lactobacillus species, and found that biofilm-forming cells of a L. fermentum strain had a significantly higher survival rate than planktonic cells in cefotaxime, cefmetazole and tetracycline, but were as sensitive to oxacillin and ampicillin as planktonic cells were.
FAO/WHO (2002) Guidelines for the Evaluation of Probiotics in Food. World Health Organization and Food and Agriculture Organization of the United Nations, London.
Pino, A., Bartolo, E., Caggia, C., Cianci, A. and Randazzo, C.L. (2019) Detection of Vaginal Lactobacilli as Probiotic Candidates. Scientific Reports, 9, Article No. 3355. https://doi.org/10.1038/s41598-019-40304-3
Dlamini, Z.C., Langa, R., Aiyegoro, O.A. and Okoh, A.I. (2019) Safety Evaluation and Colonisation Abilities of Four Lactic Acid Bacteria as Future Probiotics. Probiotics and Antimicrobial Proteins, 11, 397-402. https://doi.org/10.1007/s12602-018-9430-y
Kang, C.H., Kim, Y., Han, S.H., Kim, J.S., Paek, N.S. and So, J.S. (2018) In Vitro Probiotic Properties of Vaginal Lactobacillus fermentum MG901 and Lactobacillus plantarum MG989 against Candida albicans. European Journal of Obstetrics, Gynecology, and Reproductive Biology, 228, 232-237. https://doi.org/10.1016/j.ejogrb.2018.07.005
Leccese Terraf, M.C., Juárez Tomás, M.S., Nader-Macías, M.E. and Silva, C. (2012) Screening of Biofilm Formation by Beneficial Vaginal Lactobacilli and Influence of Culture Media Components. Journal of Applied Microbiology, 113, 1517-1529. https://doi.org/10.1111/j.1365-2672.2012.05429.x
Leccese Terraf, M.C., Juárez Tomás, M.S., Rault, L., Le Loir, Y., Even, S. and Nader-Macías, M.E. (2016) Biofilms of Vaginal Lactobacillus reuteri CRL 1324 and Lactobacillus rhamnosus CRL 1332: Kinetics of Formation and Matrix Characterization. Archives of Microbiology, 198, 689-700. https://doi.org/10.1007/s00203-016-1225-5
Nikolic, M., Jovcic, B., Kojic, M. and Topisirovic, L. (2010) Surface Properties of Lactobacillus and Leuconostoc Isolates from Homemade Cheeses Showing Auto-Aggregation Ability. European Food Research and Technology, 231, 925-931. https://doi.org/10.1007/s00217-010-1344-1
Piwat, S., Sophatha, B. and Teanpaisan, R. (2015) An Assessment of Adhesion, Aggregation and Surface Charges of Lactobacillus Strains Derived from the Human Oral Cavity. Letters in Applied Microbiology, 61, 98-105. https://doi.org/10.1111/lam.12434
Chaudhary, A. and Saharan, B.S. (2019) Probiotic Properties of Lactobacillus plantarum. Journal of Pure and Applied Microbiology, 13, 933-948. https://doi.org/10.22207/JPAM.13.2.30
Bellon-Fontaine, M.N., Rault, J. and van Oss, C.J. (1996) Microbial Adhesion to Solvents: A Novel Method to Determine the Electron-Donor/Electron-Acceptor or Lewis Acid-Base Properties of Microbial Cells. Colloids and Surfaces B: Biointerfaces, 7, 47-53. https://doi.org/10.1016/0927-7765(96)01272-6
Bove, P., Capozzi, V., Garofalo, C., Rieu, A., Spano, G. and Fiocco, D. (2012) Inactivation of the ftsH Gene of Lactobacillus plantarum WCFS1: Effects on Growth, Stress Tolerance, Cell Surface Properties and Biofilm Formation. Microbiological Research, 167, 187-193. https://doi.org/10.1016/j.micres.2011.07.001
Hall, C.W. and Mah, T.F. (2017) Molecular Mechanisms of Biofilm-Based Antibiotic Resistance and Tolerance in Pathogenic Bacteria. FEMS Microbiology Reviews, 41, 276-301. https://doi.org/10.1093/femsre/fux010
Abebe, G.M. (2020) The Role of Bacterial Biofilm in Antibiotic Resistance and Food Contamination. International Journal of Microbiology, 2020, Article ID: 1705814. https://doi.org/10.1155/2020/1705814
Chen, Y.T., Hsieh, P.S., Ho, H.H., Hsieh, S.H., Kuo, Y.W., Yang, S.F. and Lin, C.W. (2020) Antibacterial Activity of Viable and Heat-Killed Probiotic Strains against Oral Pathogens. Letters in Applied Microbiology, 70, 310-317. https://doi.org/10.1111/lam.13275
Asan-Ozusaglam, M. and Gunyakti, A. (2018) Lactobacillus fermentum Strains from Human Breast Milk with Probiotic Properties and Cholesterol-Lowering Effects. Food Science and Biotechnology, 28, 501-509. https://doi.org/10.1007/s10068-018-0494-y
Klimko, A.I., Cherdyntseva, T.A., Brioukhanov, A.L. and Netrusov, A.I. (2020) In Vitro Evaluation of Probiotic Potential of Selected Lactic Acid Bacteria Strains. Probiotics and Antimicrobial Proteins, 12, 1139-1148. https://doi.org/10.1007/s12602-019-09599-6
Salas-Jara, M.J., Sanhueza, E.A., Retamal-Díaz, A., González, C., Urrutia, H. and García, A. (2016) Probiotic Lactobacillus fermentum UCO-979C Biofilm Formation on AGS and Caco-2 Cells and Helicobacter pylori Inhibition. Biofouling, 32, 1245-1257. https://doi.org/10.1080/08927014.2016.1249367
Ahmadi, S., Wang, S., Nagpal, R., Wang, B., Jain, S., Razazan, A., Mishra, S.P., Zhu, X., Wang, Z., Kavanagh, K. and Yadav, H. (2020) A Human-Origin Probiotic Cocktail Ameliorates Aging-Related Leaky Gut and Inflammation via Modulating the Microbiota/Taurine/Tight Junction Axis. JCI Insight, 5, e132055. https://doi.org/10.1172/jci.insight.132055
Archer, A.C. and Halami, P.M. (2015) Probiotic Attributes of Lactobacillus fermentum Isolated from Human Feces and Dairy Products. Applied Microbiology and Biotechnology, 99, 8113-8123. https://doi.org/10.1007/s00253-015-6679-x
Nagpal, R., Wang, S., Ahmadi, S., Hayes, J., Gagliano, J., Subashchandrabose, S., Kitzman, D.W., Becton, T., Read, R. and Yadav, H. (2018) Human-Origin Probiotic Cocktail Increases Short-Chain Fatty Acid Production via Modulation of Mice and Human Gut Microbiome. Scientific Reports, 8, Article No. 12649. https://doi.org/10.1038/s41598-018-30114-4
Li, S.J., Jeon, J.M., Hong, S.W. and So, J.S. (2008) Comparison of Environmental Stress Tolerance between Lactobacillus fermentum Strains with High and Low Cell Surface Hydrophobicity. Food Science and Biotechnology, 17, 257-261.
Arena, M.P., Capozzi, V., Longo, A., Russo, P., Weidmann, S., Rieu, A., Guzzo, J., Spano, G. and Fiocco, D. (2019) The Phenotypic Analysis of Lactobacillus plantarum shsp Mutants Reveals a Potential Role for hsp1 in Cryotolerance. Frontiers in Microbiology, 10, 838. https://doi.org/10.3389/fmicb.2019.00838
Kirillova, A.V., Danilushkina, A.A., Irisov, D.S., Bruslik, N.L., Fakhrullin, R.F., Zakharov, Y.A., Bukhmin, V.S. and Yarullina, D.R. (2017) Assessment of Resistance and Bioremediation Ability of Lactobacillus Strains to Lead and Cadmium. International Journal of Microbiology, 2017, Article ID: 9869145. https://doi.org/10.1155/2017/9869145
Sharma, K., Attri, S. and Goel, G. (2019) Selection and Evaluation of Probiotic and Functional Characteristics of Autochthonous Lactic Acid Bacteria Isolated from Fermented Wheat Four Dough Babroo. Probiotics and Antimicrobial Proteins, 11, 774-784. https://doi.org/10.1007/s12602-018-9466-z
Aziz, K., Tariq, M. and Zaidi, A. (2019) Biofilm Development in L. fermentum under Shear Flow & Sequential GIT Digestion. FEMS Microbiology Letters, 366, fnz064. https://doi.org/10.1093/femsle/fnz064
Fernández Ramírez, M.D., Nierop Groot, M.N., Smid, E.J., Hols, P., Kleerebezem, M. and Abee, T. (2018) Role of Cell Surface Composition and Lysis in Static Biofilm Formation by Lactobacillus plantarum WCFS1. International Journal of Food Microbiology, 271, 15-23. https://doi.org/10.1016/j.ijfoodmicro.2018.02.013
Dec, M., Urban-Chmiel, R., Stępień-Pyśniak, D. and Wernicki, A. (2017) Assessment of Antibiotic Susceptibility in Lactobacillus Isolates from Chickens. Gut Pathogens, 9, 54. https://doi.org/10.1186/s13099-017-0203-z
Ishida, H., Ishida, Y., Kurosaka, Y., Otani, T., Sato, K. and Kobayashi, H. (1998) In Vitro and in Vivo Activities of Levofloxacin against Biofilm-Producing Pseudomonas aeruginosa. Antimicrobial Agents and Chemotherapy, 42, 1641-1645. https://doi.org/10.1128/AAC.42.7.1641
Ocana, V.S., Bru, E., De Ruiz Holgado, A.A. and Nader-Macias, M.E. (1999) Surface Characteristics of Lactobacilli Isolated from Human Vagina. The Journal of General and Applied Microbiology, 45, 203-212. https://doi.org/10.2323/jgam.45.203
Pelletier, C., Bouley, C., Cayuela, C., Bouttier, S., Bourlioux, P. and Bellon-Fontaine, M.N. (1997) Cell Surface Characteristics of Lactobacillus casei subsp. casei, Lactobacillus paracasei subsp. paracasei, and Lactobacillus rhamnosus Strains. Applied and Environmental Microbiology, 63, 1725-1731. https://doi.org/10.1128/AEM.63.5.1725-1731.1997
Bouridane, H., Sifour, M., Idoui, T., Annick, L. and Thonard, P. (2016) Technological and Probiotic Traits of the Lactobacilli Isolated from Vaginal Tract of the Healthy Women for Probiotic Use. Iranian Journal of Biotechnology, 14, 192-201. https://doi.org/10.15171/ijb.1432
Dimitonova, S.P., Danova, S.T., Serkedjieva, J.P. and Bakalov, B.V. (2007) Antimicrobial Activity and Protective Properties of Vaginal Lactobacilli from Healthy Bulgarian Women. Anaerobe, 13, 178-184. https://doi.org/10.1016/j.anaerobe.2007.08.003
Hütt, P., Lapp, E., Štšepetova, J., Smidt, I., Taelma, H., Borovkova, N., Oopkaup, H., Ahelik, A., Rööp, T., Hoidmets, D., Samuel, K., Salumets, A. and Mändar, R. (2016) Characterisation of Probiotic Properties in Human Vaginal Lactobacilli Strains. Microbial Ecology in Health and Disease, 27, 30484. https://doi.org/10.3402/mehd.v27.30484
Kmet, V. and Lucchini, F. (1997) Aggregation-Promoting Factor in Human Vaginal Lactobacillus Strains. FEMS Immunology and Medical Microbiology, 19, 111-114. https://doi.org/10.1111/j.1574-695X.1997.tb01079.x
Malik, S., Petrova, M.I., Claes, I.J., Verhoeven, T.L., Busschaert, P., Vaneechoutte, M., Lievens, B., Lambrichts, I., Siezen, R.J., Balzarini, J., Vanderleyden, J. and Lebeer, S. (2013) The Highly Autoaggregative and Adhesive Phenotype of the Vaginal Lactobacillus plantarum Strain CMPG5300 Is Sortase Dependent. Applied and Environmental Microbiology, 79, 4576-4585. https://doi.org/10.1128/AEM.00926-13
Fuochi, V., Cardile, V., Petronio Petronio, G. and Furneri, P.M. (2019) Biological Properties and Production of Bacteriocins-like-Inhibitory Substances by Lactobacillus sp. Strains from Human Vagina. Journal of Applied Microbiology, 126, 1541-1550. https://doi.org/10.1111/jam.14164
Nissilä, E., Douillard, F.P., Ritari, J., Paulin, L., Järvinen, H.M., Rasinkangas, P., Haapasalo, K., Meri, S., Jarva, H. and de Vos, W.M. (2017) Correction: Genotypic and Phenotypic Diversity of Lactobacillus rhamnosus Clinical Isolates, Their Comparison with Strain GG and Their Recognition by Complement System. PLoS ONE, 12, e0181292. https://doi.org/10.1371/journal.pone.0181292