Abstract
Oxalobacter formigenes is a unique intestinal organism that relies on oxalate degradation to meet most of its energy and carbon needs. A lack of colonization is a risk factor for calcium oxalate stone disease. Protection against calcium oxalate stone disease appears to be due to the oxalate degradation that occurs in the gut on low calcium diets with a possible further contribution from intestinal oxalate secretion. Much remains to be learned about how the organism establishes and maintains gut colonization and the precise mechanisms by which it modifies stone risk. The sequencing and annotation of the genomes of a Group 1 and a Group 2 strain of O. formigenes should provide the informatic tools required for the identification of the genes and pathways associated with colonization and survival. In this review we have identified genes that may be involved and where appropriate suggested how they may be important in calcium oxalate stone disease. Elaborating the functional roles of these genes should accelerate our understanding of the organism and clarify its role in preventing stone formation.
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References
Allison MJ, Cook HM (1981) Oxalate degradation by microbes of the large bowel of herbivores: the effect of dietary oxalate. Science 212:675–676
Allison MJ, Littledike ET, James LF (1977) Changes in ruminal oxalate degradation rates associated with adaptation to oxalate ingestion. J Anim Sci 45:1173–1179
Anantharam V, Allison MJ, Maloney PC (1989) Oxalate:formate exchange. The basis for energy coupling in Oxalobacter. J Biol Chem 264:7244–7250
Argenzio RA, Liacos JA, Allison MJ (1988) Intestinal oxalate-degrading bacteria reduce oxalate absorption and toxicity in guinea pigs. J Nutr 118:787–792
Arnold KW, Kaspar CW (1995) Starvation- and stationary-phase-induced acid tolerance in Escherichia coli O157:H7. Appl Environ Microbiol 61:2037–2039
Baetz AL, Allison MJ (1989) Purification and characterization of oxalyl-coenzyme A decarboxylase from Oxalobacter formigenes. J Bacteriol 171:2605–2608
Baetz AL, Allison MJ (1990) Purification and characterization of formyl-coenzyme A transferase from Oxalobacter formigenes. J Bacteriol 172:3537–3540
Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S (2004) Bacterial persistence as a phenotypic switch. Science 305:1622–1625
Batislam E, Yilmaz E, Yuvanc E, Kisa O, Kisa U (2012) Quantitative analysis of colonization with real-time PCR to identify the role of Oxalobacter formigenes in calcium oxalate urolithiasis. Urol Res 40:455–460
Bentley SD, Parkhill J (2004) Comparative genomic structure of prokaryotes. Annu Rev Genet 38:771–792
Capitani G, Eidam O, Glockshuber R, Grutter MG (2006) Structural and functional insights into the assembly of type 1 pili from Escherichia coli. Microbes Infect 8(8):2284–2290
Capra EJ, Laub MT (2012) Evolution of two-component signal transduction systems. Annu Rev Microbiol 66:325–347
Cascales E, Buchanan SK, Duche D, Kleanthous C, Lloubes R, Postle K, Riley M, Slatin S, Cavard D (2007) Colicin biology. Microbiol Mol Biol Rev 71:158–229
Connon SA, Tovanabootr A, Dolan M, Vergin K, Giovannoni SJ, Semprini L (2005) Bacterial community composition determined by culture-independent and -dependent methods during propane-stimulated bioremediation in trichloroethene-contaminated groundwater. Environ Microbiol 7:165–178
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
Cornick NA, Allison MJ (1996) Anabolic incorporation of oxalate by Oxalobacter formigenes. Appl Environ Microbiol 62:3011–3013
Cornick NA, Allison MJ (1996) Assimilation of oxalate, acetate, and CO2 by Oxalobacter formigenes. Can J Microbiol 42:1081–1086
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
Ditto MD, Roberts D, Weisberg RA (1994) Growth phase variation of integration host factor level in Escherichia coli. J Bacteriol 176:3738–3748
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
Ellison DW, Miller VL (2006) Regulation of virulence by members of the MarR/SlyA family. Curr Opin Microbiol 9:153–159
Franceschi VR (1989) Calcium oxalate formation is a rapid and reversible process in Lemna minor L. Protoplasma 148:130–137
Freel RW, Hatch M, Green M, Soleimani M (2006) Ileal oxalate absorption and urinary oxalate excretion are enhanced in Slc26a6 null mice. Am J Physiol Gastrointest Liver Physiol 290:G719–G728
Garneau JE, Dupuis ME, Villion M, Romero DA, Barrangou R, Boyaval P, Fremaux C, Horvath P, Magadan AH, Moineau S (2010) The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468:67–71
Givskov M, Eberl L, Moller S, Poulsen LK, Molin S (1994) Responses to nutrient starvation in Pseudomonas putida KT2442: analysis of general cross-protection, cell shape, and macromolecular content. J Bacteriol 176:7–14
Gottesman S, Storz G (2011) Bacterial small RNA regulators: versatile roles and rapidly evolving variations. Cold Spring Harb Perspect Biol 3(12)
Hansen AM, Gu Y, Li M, Andrykovitch M, Waugh DS, Jin DJ, Ji X (2005) Structural basis for the function of stringent starvation protein a as a transcription factor. J Biol Chem 280:17380–17391
Hatch M, Gjymishka A, Salido EC, Allison MJ, Freel RW (2011) Enteric oxalate elimination is induced and oxalate is normalized in a mouse model of primary hyperoxaluria following intestinal colonization with Oxalobacter. Am J Physiol Gastrointest Liver Physiol 300:G461–G469
Holmes RP, Assimos DG (2004) The impact of dietary oxalate on kidney stone formation. Urol Res 32:311–316
Hoppe B, Groothoff JW, Hulton SA, Cochat P, Niaudet P, Kemper MJ, Deschenes G, Unwin R, Milliner D (2011) Efficacy and safety of Oxalobacter formigenes to reduce urinary oxalate in primary hyperoxaluria. Nephrol Dial Transplant 26:3609–3615
Ilarslan H, Palmer RG, Horner HT (2001) Calcium oxalate crystals in developing seeds of soybean. Ann Bot 88:243–257
Ilarslan H, Palmer RG, Imsande J, Horner HT (1997) Quantitative determination of calcium oxalate and oxalate in developing seeds of soybean (Leguminosae). Am J Bot 84:1042–1046
Jenkins DE, Chaisson SA, Matin A (1990) Starvation-induced cross protection against osmotic challenge in Escherichia coli. J Bacteriol 172:2779–2781
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
Kang DC, Venkataraman PA, Dumont ME, Maloney PC (2011) Oligomeric state of the oxalate transporter, OxlT. Biochemistry 50:8445–8453
Kaufman DW, Kelly JP, Curhan GC, Anderson TE, Dretler SP, Preminger GM, Cave DR (2008) Oxalobacter formigenes may reduce the risk of calcium oxalate kidney stones. J Am Soc Nephrol 19:1197–1203
Kelly JP, Curhan GC, Cave DR, Anderson TE, Kaufman DW (2011) Factors related to colonization with Oxalobacter formigenes in U.S. adults. J Endourol 25:673–679
Kharlamb V, Schelker J, Francois F, Jiang J, Holmes RP, Goldfarb DS (2011) Oral antibiotic treatment of Helicobacter pylori leads to persistently reduced intestinal colonization rates with Oxalobacter formigenes. J Endourol 25:1781–1785
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
Landgraf JR, Wu J, Calvo JM (1996) Effects of nutrition and growth rate on Lrp levels in Escherichia coli. J Bacteriol 178:6930–6936
Lange JN, Wood KD, Wong H, Otto R, Mufarrij PW, Knight J, Akpinar H, Holmes RP, Assimos DG (2012) Sensitivity of human strains of Oxalobacter formigenes to commonly prescribed antibiotics. Urology 79:1286–1289
Lindahl A, Ungell AL, Knutson L, Lennernas H (1997) Characterization of fluids from the stomach and proximal jejunum in men and women. Pharm Res 14:497–502
Mittal RD, Kumar R, Bid HK, Mittal B (2005) Effect of antibiotics on Oxalobacter formigenes colonization of human gastrointestinal tract. J Endourol 19:102–106
Mj A, Ka D, Wr M, Jg F (1985) Oxalobacter formigenes gen. nov., sp. nov.: oxalate-degrading anaerobes that inhabit the gastrointestinal tract. Arch Microbiol 141:1–7
Muller JA, Ross RP, Sybesma WF, Fitzgerald GF, Stanton C (2011) Modification of the technical properties of Lactobacillus johnsonii NCC 533 by supplementing the growth medium with unsaturated fatty acids. Appl Environ Microbiol 77:6889–6898
Nasser W, Reverchon S (2007) New insights into the regulatory mechanisms of the LuxR family of quorum sensing regulators. Anal Bioanal Chem 387:381–390
Navarro Llorens JM, Tormo A, Martinez-Garcia E (2010) Stationary phase in gram-negative bacteria. FEMS Microbiol Rev 34:476–495
Nguyen D, Joshi-Datar A, Lepine F, Bauerle E, Olakanmi O, Beer K, McKay G, Siehnel R, Schafhauser J, Wang Y, Britigan BE, Singh PK (2011) Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science 334:982–986
Palgi N, Ronen Z, Pinshow B (2008) Oxalate balance in fat sand rats feeding on high and low calcium diets. J Comp Physiol B 178:617–622
Rebuffat S (2012) Microcins in action: amazing defence strategies of Enterobacteria. Biochem Soc Trans 40:1456–1462
Roberts RB, Abelson PH, Cowie D, Bolton ET, Britten RJ (1955) Studies of Biosynthesis in Escherichia coli. Carnegie Institution of Washington Publication, Washington DC
Ruan ZS, Anantharam V, Crawford IT, Ambudkar SV, Rhee SY, Allison MJ, Maloney PC (1992) Identification, purification, and reconstitution of OxlT, the oxalate: formate antiport protein of Oxalobacter formigenes. J Biol Chem 267:10537–10543
Sidhu H, Hoppe B, Hesse A, Tenbrock K, Bromme S, Rietschel E, Peck AB (1998) Absence of Oxalobacter formigenes in cystic fibrosis patients: a risk factor for hyperoxaluria. Lancet 352:1026–1029
Sidhu H, Schmidt ME, CorneliusT JG, Thamiselvam S, Khan SR, Hesse A, Peck AB (1999) Direct correlation between hyperoxaluria/oxalate stone disease and the absence of the gastrointestinal tract dwelling bacterium Oxalobacter formigenes: possible prevention by gut recolonization or enzyme replacement therapy. J Am Soc Nephrol 10:S334–S340
Sidhu H, Yenatska L, Ogden SD, Allison MJ, Peck AB (1997) Natural colonization of children in the Ukraine with the intestinal bacterium, Oxalobacter formigenes, using a PCR-based detection system. Mol Diagn 2:89–97
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. Kid Int
Song HK, Eck MJ (2003) Structural basis of degradation signal recognition by SspB, a specificity-enhancing factor for the ClpXP proteolytic machine. Mol Cell 12:75–86
Troxel SA, Sidhu H, Kaul P, Low RK (2003) Intestinal Oxalobacter formigenes colonization in calcium oxalate stone formers and its relation to urinary oxalate. J Endourol
Wang X, Kim Y, Ma Q, Hong SH, Pokusaeva K, Sturino JM, Wood TK (2010) Cryptic prophages help bacteria cope with adverse environments. Nat Commun 1:147
Weaver GA, Krause JA, Allison MJ, Lindenbaum J (1992) Distribution of digoxin-reducing, oxalate-degrading, and total anaerobic bacteria in the human colon. Microb Ecol Health D 5:227–234
Weber H, Polen T, Heuveling J, Wendisch VF, Hengge R (2005) Genome-wide analysis of the general stress response network in Escherichia coli: sigmaS-dependent genes, promoters, and sigma factor selectivity. J Bacteriol 187:1591–1603
Wei Y, Perez LJ, Ng WL, Semmelhack MF, Bassler BL (2011) Mechanism of Vibrio cholerae autoinducer-1 biosynthesis. ACS Chem Biol 6:356–365
Williams MD, Ouyang TX, Flickinger MC (1994) Starvation-induced expression of SspA and SspB: the effects of a null mutation in sspA on Escherichia coli protein synthesis and survival during growth and prolonged starvation. Mol Microbiol 11:1029–1043
Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS (2011) PHAST: a fast phage search tool. Nucleic Acids Res 39:W347–W352
Acknowledgments
This research was supported in part by NIH grants DK087967 and DK062284. The “Oxalobacter formigenes Sequencing Project, Broad Institute of Harvard and MIT (http://www.broadinstitute.org/)” and the Integrated Microbial Genomes (IMG) system, supported by the NIH Human Microbiome Project, were used for genomic data analysis.
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Knight, J., Deora, R., Assimos, D.G. et al. The genetic composition of Oxalobacter formigenes and its relationship to colonization and calcium oxalate stone disease. Urolithiasis 41, 187–196 (2013). https://doi.org/10.1007/s00240-013-0566-7
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DOI: https://doi.org/10.1007/s00240-013-0566-7