Abstract
Oxalobacter formigenes (O. formigenes) is a nonpathogenic, Gram-negative, obligate anaerobic bacterium that commonly inhabits the human gut and degrades oxalate as its major energy and carbon source. Results from a case-controlled study suggested that lack of O. formigenes colonization is a risk factor for recurrent calcium oxalate stone formation. Hence, O. formigenes colonization may prove to be an efficacious method for limiting calcium oxalate stone risk. However, challenges exist in the preparation of O. formigenes as a successful probiotic due to it being an anaerobe with fastidious growth requirements. Here we examine in vitro properties expected of a successful probiotic strain. The data show that the Group 1 O. formigenes strain OxCC13 is sensitive to pH < 5.0, persists in the absence of oxalate, is aerotolerant, and survives for long periods when freeze-dried or mixed with yogurt. These findings highlight the resilience of this O. formigenes strain to some processes and conditions associated with the manufacture, storage and distribution of probiotic strains.
References
Allison MJ, Dawson KA, Mayberry WR, Foss JG (1985) Oxalobacter formigenes gen. nov., sp. nov.: oxalate-degrading anaerobes that inhabit the gastrointestinal tract. Arch Microbiol 141:1–7
Argenzio RA, Liacos JA, Allison MJ (1988) Intestinal oxalate-degrading bacteria reduce oxalate absorption and toxicity in guinea pigs. J Nutr 118:787–792
Barnett C, Nazzal L, Goldfarb DS, Blaser MJ (2015) The presence of Oxalobacter formigenes in the microbiome of healthy young adults. J Urol. doi:10.1016/j.juro.2015.08.070
Bezkorovainy A (2001) Probiotics: determinants of survival and growth in the gut. Am J Clin Nutr 73:399S–405S
Biavati B, Sozzi T, Mattarelli P, Trovatelli LD (1992) Survival of bifidobacteria from human habitat in acidified milk. Microbiologica 15:197–200
Celik OF, O’Sullivan DJ (2013) Factors influencing the stability of freeze-dried stress-resilient and stress-sensitive strains of bifidobacteria. J Dairy Sci 96:3506–3516. doi:10.3168/jds.2012-6327
Cornelius JG, Peck AB (2004) Colonization of the neonatal rat intestinal tract from environmental exposure to the anaerobic bacterium Oxalobacter formigenes. J Med Microbiol 53:249–254
Daniel SL, Hartman PA, Allison MJ (1987) Intestinal colonization of laboratory rats with Oxalobacter formigenes. Appl Environ Microbiol 53:2767–2770
Dawson KA, Allison MJ, Hartman PA (1980) Isolation and some characteristics of anaerobic oxalate-degrading bacteria from the rumen. Appl Environ Microbiol 40:833–839
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
Ellis ML, Shaw KJ, Jackson SB, Daniel SL, Knight J (2015) Analysis of commercial kidney stone probiotic supplements. Urology 85:517–521
Ellis ME, Mobley JA, Holmes RP, Knight J (2016) Proteome dynamics of the specialist oxalate degrader. J Proteomics Bioinform 9:19–24. doi:10.4172/jpb.1000384
Fisberg M, Machado R (2015) History of yogurt and current patterns of consumption. Nutr Rev 73(Suppl 1):4–7. doi:10.1093/nutrit/nuv020
Gregory EM, Moore WE, Holdeman LV (1978) Superoxide dismutase in anaerobes: survey. Appl Environ Microbiol 35:988–991
Hatch M, Freel RW (2013) A human strain of Oxalobacter (HC-1) promotes enteric oxalate secretion in the small intestine of mice and reduces urinary oxalate excretion. Urolithiasis 41:379–384. doi:10.1007/s00240-013-0601-8
Hatch M, Cornelius J, Allison M, Sidhu H, Peck A, Freel RW (2006) Oxalobacter sp. reduces urinary oxalate excretion by promoting enteric oxalate secretion. Kidney Int 69:691–698. doi:10.1038/sj.ki.5000162
Hewitt J, Morris JG (1975) Superoxide dismutase in some obligately anaerobic bacteria. FEBS Lett 50:315–318
Hoppe B et al (2006) Oxalobacter formigenes: a potential tool for the treatment of primary hyperoxaluria type 1. Kidney Int 70:1305–1311. doi:10.1038/sj.ki.5001707
Hoppe B et al (2011) Efficacy and safety of Oxalobacter formigenes to reduce urinary oxalate in primary hyperoxaluria. Nephrol Dial Transplant 26:3609–3615. doi:10.1093/ndt/gfr107
Jiang J, Knight J, Easter LH, Neiberg R, Holmes RP, Assimos DG (2011) Impact of dietary calcium and oxalate, and Oxalobacter formigenes colonization on urinary oxalate excretion. J Urol 186:135–139. doi:10.1016/j.juro.2011.03.006
Kaufman DW et al (2008) Oxalobacter formigenes may reduce the risk of calcium oxalate kidney stones. J Am Soc Nephrol 19:1197–1203. doi:10.1681/ASN.2007101058
Knight J, Deora R, Assimos DG, Holmes RP (2013) The genetic composition of Oxalobacter formigenes and its relationship to colonization and calcium oxalate stone disease. Urolithiasis 41:187–196. doi:10.1007/s00240-013-0566-7
Kuhner CH, Hartman PA, Allison MJ (1996) Generation of a proton motive force by the anaerobic oxalate-degrading bacterium Oxalobacter formigenes. Appl Environ Microbiol 62:2494–2500
Leszczynska D, Matuszewska E, Kuczynska-Wisnik D, Furmanek-Blaszk B, Laskowska E (2013) The formation of persister cells in stationary-phase cultures of Escherichia coli is associated with the aggregation of endogenous proteins. PLoS ONE 8:e54737. doi:10.1371/journal.pone.0054737
Li X, Ellis ML, Knight J (2015) Oxalobacter formigenes colonization and oxalate dynamics in a mouse model. Appl Environ Microbiol 81:5048–5054. doi:10.1128/AEM.01313-15
Liu Y, Tang H, Lin Z, Xu P (2015) Mechanisms of acid tolerance in bacteria and prospects in biotechnology and bioremediation. Biotechnol Adv 33:1484–1492. doi:10.1016/j.biotechadv.2015.06.001
Loesche WJ (1969) Oxygen sensitivity of various anaerobic bacteria. Appl Microbiol 18:723–727
Lu P et al (2013) l-glutamine provides acid resistance for Escherichia coli through enzymatic release of ammonia. Cell Res 23:635–644. doi:10.1038/cr.2013.13
Miller AW, Kohl KD, Dearing MD (2014) The gastrointestinal tract of the white-throated Woodrat (Neotoma albigula) harbors distinct consortia of oxalate-degrading bacteria. Appl Environ Microbiol 80:1595–1601. doi:10.1128/AEM.03742-13
Miyamoto-Shinohara Y, Sukenobe J, Imaizumi T, Nakahara T (2008) Survival of freeze-dried bacteria. J Gen Appl Microbiol 54:9–24
Rocha ER, Selby T, Coleman JP, Smith CJ (1996) Oxidative stress response in an anaerobe, Bacteroides fragilis: a role for catalase in protection against hydrogen peroxide. J Bacteriol 178:6895–6903
Rozen DE, Philippe N, Arjan de Visser J, Lenski RE, Schneider D (2009) Death and cannibalism in a seasonal environment facilitate bacterial coexistence. Ecol Lett 12:34–44. doi:10.1111/j.1461-0248.2008.01257.x
Shah NP (2000) Probiotic bacteria: selective enumeration and survival in dairy foods. J Dairy Sci 83:894–907. doi:10.3168/jds.S0022-0302(00)74953-8
Siener R, Bangen U, Sidhu H, Honow R, von Unruh G, Hesse A (2013) The role of Oxalobacter formigenes colonization in calcium oxalate stone disease. Kidney Int 83:1144–1149. doi:10.1038/ki.2013.104
Talwalkar A, Kailasapathy K (2004) The role of oxygen in the viability of probiotic bacteria with reference to L. acidophilus and Bifidobacterium spp. Curr Issues Intest Microbiol 5:1–8
Zambrano MM, Siegele DA, Almiron M, Tormo A, Kolter R (1993) Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science 259:1757–1760
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This work was supported by National Institutes of Health (NIH) grant DK087967.
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Communicated by Erko Stackebrandt.
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Ellis, M.L., Dowell, A.E., Li, X. et al. Probiotic properties of Oxalobacter formigenes: an in vitro examination. Arch Microbiol 198, 1019–1026 (2016). https://doi.org/10.1007/s00203-016-1272-y
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DOI: https://doi.org/10.1007/s00203-016-1272-y