Abstract
Kidney stones composed of oxalate are a significant health problem. It has been suggested that modification of the intestinal microbiota to reduce the amount of oxalate in the digestive system could be an effective treatment. There have been several studies into the use of lactic acid bacteria for the degradation of intestinal oxalates. We isolated 88 lactic acid bacteria strains from a range of dairy products, and screened for their ability to degrade oxalate. Using the oxalate-degrading Enzymatic Activity Index and the viable cell counts, five strains of Lactobacillus fermentum and two strains of Lactobacillus gastricus were identified as having strong oxalate degradation abilities, and were further investigated. All seven strains were able to tolerate acid (pH 4 and 3), bile salts (0.3%), phenol (0.3%), and to produce exopolysaccharides. They were resistant to a wide range of antibiotics. Among these strains, Lactobacillus fermentum NRAMJ5 and Lactobacillus gastricus NRAMJ2 were, therefore, good candidates as probiotics for managing hyperoxaluria.
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References
Afriani, Arnim A, Yetti M, Yuherman (2018) Isolation and characterization of lactic acid bacteria proteases from Bekasam for use as a beef tenderizer. Pak J Nutr. 17: 361-367. https://doi.org/10.3923/pjn.2018.361.367
Allison MJ, Dawson KA, Mayberry WR, Foss JG (1985) Oxalobacter formigenesgen.nov., sp. nov.: oxalate-degrading anaerobes that inhabit the gastrointestinal tract. Arch Microbiol 141:1–7. https://doi.org/10.1007/BF00446731
Anandharaj M, Sivasankari B (2014) Isolation of potential probiotic Lactobacillus oris HMI68 from mother’s milk with cholesterol-reducing property. J Biosci p1:7. https://doi.org/10.1016/j.jbiosc.2014.01.015
Atanassova M, Choiset Y, Dalgalarrondo M, Chobert J M, Dousset X, Ivanova I, Haertle T (2003) Isolation and partial biochemical characterization of a proteinaceous anti-bacteria and anti-yeast compound produced by Lactobacillus paracaseisubsp. paracaseistrain M3. Int J Food Microbiol 87:6373. https://doi.org/10.1016/S0168-1605(03)00054-0
Awan J A, Rahman S U (2005) Microbiology Manual. Unitech Communications, Faisalabad, Pakistan, pp 49–51.
Bao Y, Zhang Y, Zhang Y, Liu Y, Wang S, Dong X (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
Campieri C, Campieri M, Bertuzzi V, Swennen E, Mateeuzzi D, Stefoni S, Pirovano F, Centi C, Ulisse S, Famularo G, De Simone C (2001) Reduction of oxaluria after an oral course of lactic acid bacteria at high concentration. Kidney Int 60:1097–1105. https://doi.org/10.1046/j.1523-1755.2001.0600031097.x
Chamberlain CA, Hatch M, Garrett TJ (2019) Metabolomic profiling of oxalate-degrading probiotic Lactobacillus acidophilus and Lactobacillus gasseri. PLos one 14(9). https://doi.org/10.1371/journal.pone.0222393
Charteris WP, Kelly PM, Morelli L, Collins JK (1998) Development and application of an in-vitro methodology to determine the transit tolerance of potentially probiotic Lactobacillus and Bifidobacterium species in upper gastrointestinal tract. J Appl Microbiol 84:759–768. https://doi.org/10.1046/j.1365-2672.1998.00407.x
Clinical and Laboratory Standards Institute (CLSI) (2009): Performance standard for antimicrobial disk susceptibility tests, M2-A10. CLSI, Wayne, PA, USA.
Conter M, Muscariello T, Zanardi E, Ghidini S, Vergara A, Campanini G, Lanieri A (2005) Characterization of lactic acid bacteria isolated from an italian dry fermented sausage. Romn Biotechnol Lett 14:167–174. https://doi.org/10.1016/S0309-1740(02)00292-9
Corcoran BM, Stanton C, Fitzgerald GF, Ross RP (2005) Survival of probiotic lactobacilli in acidic environments is enhanced in the presence of metabolizable sugars. Appl Environ Microbiol 71:3060–3067. https://doi.org/10.1128/AEM.71.6.3060-3067.2005
Crescenzi V (1995) Microbial polysaccharides of applied interest: ongoing research activities in Europe. Biotechnol Prog 11:251–259. https://doi.org/10.1021/bp00033a002
De Vuyst L, Makras L, Avonts L, Holo H, Yi Q, Dhanasekaran D, Sakthi V, Thajuddin N, Panneerselvam A (2004) Preliminary evaluation of Anopheles mosquito larvicidal efficacy of mangrove actinobacteria. Int J Appl Biol PharmTechnol 1:374–381
Duncan SH, Richardson AJ, Kaul P, Holmes RP, Allison MJ, Stewart CS (2002) Oxalobacter formigenes and its potential role in human health. Appl Environ Microbiol 68:3841–3847. https://doi.org/10.1128/AEM.68.8.3841-3847.2002
Dunne C, O’Mahony L, Murphy L, Thornton G, Morrissey D, O’Halloran S, Kiely B (2001) In vitro selection criteria for probiotic bacteria of human origin: correlation with in vivo findings. Am J Clin Nutr 73:386–392. https://doi.org/10.1093/ajcn/73.2.386s
El-Shafei K, Abd El-Gawad MAM, Dabiza N, Sharaf OM, Effat BA (2008) Mixed culture of Propionibacterium thoenii P-127, Lactobacillus rhamnosus and Lactobacillus plantarum as protective cultures in Kareish cheese. Polish J Food Nutr Sci 58:433–441
FAO/WHO (2006) Probiotics in food health and nutritional properties and guidelines for evaluation. FAO Food Nutr Pap 85:1–56
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.2307/2408678
Forhad MH, Rahman SMK, Rahman MDS, Saikot FK, Biswas KC (2015) Probiotic properties analysis of isolated lactic acid bacteria from buffalo milk. Arch Clin Microbiol 7:1
Georgievaa R, Yochevab L, Tserovskab L, Zhelezovab G, Stefanovaa N, Atanasovaa A, Dangulevaa A, Ivanovaa G, Karapetkova N, Rumyana N, Karaivanovaa E (2015) Antimicrobial activity and antibiotic susceptibility of Lactobacillus and Bifidobacterium spp. intended for use as starter and probiotic cultures. Biotechnol Biotechnol Equip 29: 8491. https://doi.org/10.1080/13102818.2014.987450
Gill HS, Guarner F (2004) Probiotics and human health: a clinical perspective. Postgrad Med J 80:516–526. https://doi.org/10.1136/pgmj.2003.008664
Gomathi S, Sasikumar P, Anbazhagan K, Sasikumar S, Kavitha M, Selvi M, Selvam G (2014) Screening of indigenous oxalate degrading lactic acid bacteria from human faeces and south indian fermented foods: assessment of probiotic potential. Sci World J 2014:648059. https://doi.org/10.1155/2014/648059
Gu RX, Yang ZQ, Li ZH, Chen SL, Luo ZL (2008) Probiotic properties of lactic acid bacteria isolated from stool samples of longevous people in regions of Hotan, Xinjiang and Bama, Guangxi, China. Anaerobe 14:313–317. https://doi.org/10.1016/j.anaerobe.2008.06.001
Guo LD, Wang LQ, Liu F, Li BL, Tang Y, Yu SF, Zhang DQ, Huo GC (2019) Effect of bile salt hydrolase-active Lactobacillus plantarum KLDS 1.0344 on cholesterol metabolism in rats fed a high-cholesterol diet. J Funct Foods 61:1–6. https://doi.org/10.1016/j.jff.2019.103497
Heredia-Castro PY, Méndez-Romero JI, Hernández-Mendoza A, Acedo-Félix E, González-Córdova AF, Vallejo-Cordoba B (2017) Antimicrobial activity and partial characterization of bacteriocin like inhibitory substances produced by Lactobacillus spp. isolated from artisanal Mexican cheese. J Dairy Sci 98:8285–8293. https://doi.org/10.3168/jds.2015-10104
Herrero M, Mayo B, González B, Suárez JE (1996) Evaluation of technologically important traits in lactic acid bacteria isolated from spontaneous fermentations. J Appl Bacteriol 81:565–570. https://doi.org/10.1111/j.1365-2672.1996.tb03548.x
Holmes RP, Assimos DG (1998) Glyoxylate synthesis, and its modulation and influence on oxalate synthesis. J Urol 160:1617–1624. https://doi.org/10.1016/S0022-5347(01)62363-2
Hoppe B, Beck BB, Milliner DS (2009) The primary hyperoxalurias. Kidney Int 75:1264–1271. https://doi.org/10.1038/ki.2009.32
Ito H, Kotake T, Masai M (1996) In vitro degradation of oxalic acid by human feces. Int J Urol 3:207–211. https://doi.org/10.1111/j.1442-2042.1996.tb00518.x
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Lee PKC, Cheng TCE, Yeung ACL, Lai Kh (2011) An empirical study of transformational leadership, team performance and service quality in retail banks. J Omega 39:690–701. https://doi.org/10.1016/j.omega.2011.02.001
Li W, Ji J, Rui X, Yu J, Tang W, Chen X, Dong M (2014) Production of exopolysaccharides by Lactobacillus helveticus MB2-1 and its functional characteristics in vitro. LWT - Food Sci Technol 59:732–739. https://doi.org/10.1016/j.lwt.2014.06.063
Lieske JC, Goldfarb DS, de Simone C, Regnier C (2005) Use of a probiotic to decrease enteric hyperoxaluria. Kidney Int 68:1244–1249. https://doi.org/10.1111/j.1523-1755.2005.00520.x
Lieske JC, Tremaine WJ, de Simone C, O’Connor HM, Li X, Bergstralh EJ, Goldfarb DS (2010) Diet, but not oral probiotics, effectively reduces urinary oxalate excretion and calcium oxalate supersaturation. Kidney Int 78:1178–1185. https://doi.org/10.1038/ki.2010.310
Miller AW, Dearing D (2013) The metabolic and ecological interactions of oxalate-degrading bacteria in the Mammalian gut. Pathogens 2:636–652. https://doi.org/10.3390/pathogens2040636
Murphy C, Murphy S, O’Brien F, O’Donoghue M, Boileau T, Sunvold G, Reinhart G, Kiely B, Shanahan F, O’Mahony L (2007) Metabolic activity of probiotics—oxalate degradation. Vet Microbiol 136:0378–1135. https://doi.org/10.1016/j.vetmic.2008.10.005
Murru N, Blaiotta G, Peruzy MF, Santonicola S, Mercogliano R, Aponte M (2017) Screening of oxalate degrading lactic acid bacteria of food origin. Ital J Food Saf 6(2):6345. https://doi.org/10.4081/ijfs.2017.6345
Okombo J, Liebman M (2010) Probiotic-induced reduction of gastrointestinal oxalate absorption in healthy subjects. Urol Res 38:169–178. https://doi.org/10.1007/s00240-010-0262-9
Oleksy M, Klewicka E (2016) Exopolysaccharides produced by Lactobacillus sp.: Biosynthesis and applications. Crit Rev Food Sci Nutr 1–13. https://doi.org/10.1080/10408398.2016.1187112
Pringsulaka O, Thangnagam N, Suwannasai N, Atthakor W, Pothivejkul K, Rangsiruji K (2012) Partial characterization of bacteriocins produced by lactic acid bacteria isolated from Thai fermented meat and fish products. Food Control 23:547–551. https://doi.org/10.1016/j.foodcont.2011.08.029
R€onnqvist D, Forsgren-Brusk U, Husmark U, GrahnHakansson E (2007) Lactobacillus fermentum Ess-1 with unique growth inhibition of vulvo-vaginal candidiasis pathogens. J Med Microbiol 56:1500-1504. https://doi.org/10.1099/jmm.0.47226-0
Sadaf H, Raza SI, Hassan SW (2017) Role of gut microbiota against calcium oxalate. Microb Pathog 109:287–291. https://doi.org/10.1016/j.micpath.2017.06.009
Stanford J, Charlton K, Stefoska-Needham A, Ibrahim R, Lambert K (2020) The gut microbiota profile of adults with kidney disease and kidney stones: a systematic review of the literature. BMC Nephrol 21(1):215. https://doi.org/10.1186/s12882-020-01805-w
Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Nati Acad Sci USA 101:11030–11035. https://doi.org/10.1073/pnas.0404206101
Tavasoli S, Alebouyeh M, Naji M, Shakiba M, Shabani G, Nashtaei M, Broumandnia N, Basiri A (2020) Association of intestinal oxalate-degrading bacteria with recurrent calcium kidney stone formation and hyperoxaluria: a case-control study. BJU Int 125:133–143. https://doi.org/10.1111/bju.14840
Teuber M, Meile L, Schwarz F (1999) Acquired antibiotic resistance in lactic acid bacteria from food. Antonie Van Leeuwenhoek 76:115–137. https://doi.org/10.1023/A:1002035622988
Tropcheva R, Nikolova D, Evstatieva Y, Danova S (2014) Antifungal activity and identification of Lactobacilli, isolated from traditional dairy product “katak”. Anaerobe 28:78–84. https://doi.org/10.1016/j.anaerobe.2014.05.010
Tserovska L, Stefanova S, Yordanova T (2002) Identification of lactic acid bacteria isolated from katyk, goat’s milk and cheese. J of Culture Collections 3:48–52
Turroni S, Vitali B, Bendazzoli C (2007) Oxalate consumption by lactobacilli: evaluation of oxalyl-CoA decarboxylase and formyl-CoA transferase activity in Lactobacillus acidophilus. J Appl Microbiol 103:1600–1609. https://doi.org/10.1111/j.1365-2672.2007.03388.x
Turroni S, Bendazzoli C, Samuele C, Dipalo F, Candela M, Vitali B, Gotti R, Brigidi P (2010) Oxalate-degrading activity in Bifidobacterium animalis subsp. lactis: impact of acidic conditions on the transcriptional levels of the oxalyl coenzyme A (CoA) decarboxylase and Formyl-CoA transferase genes. Appl Environl Microbiol 76:5609–5620. https://doi.org/10.1128/AEM.00844-10
Xanthopoulos V, Litopoulou-Tzanetaki E, Tzanetakis N (2000) Characterisation of Lactobacillus isolates from infant faeces as dietary adjuncts Food. Microbiol 17:205–215. https://doi.org/10.1006/fmic.1999.0300
Yadav H, Jain S, Sinha P (2007) Production of free fatty acids and conjugated linoleic acid in probiotic dahi containing Lactobacillus acidophilus and Lactobacillus casei during fermentation and storage. Intl Dairy J 17:1006–1010. https://doi.org/10.1016/j.idairyj.2006.12.003
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NS performed the experiments and all authors wrote the manuscript, analyzed the data. BE, NM, NT, MI guided the experiments and all authors revised the manuscript.
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Communicated by Erko Stackebrandt.
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Soliman, N.R., Effat, B.A.M., Mehanna, N.S. et al. Activity of probiotics from food origin for oxalate degradation. Arch Microbiol 203, 5017–5028 (2021). https://doi.org/10.1007/s00203-021-02484-3
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DOI: https://doi.org/10.1007/s00203-021-02484-3