Biology:Oxalobacter formigenes

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Short description: Species of bacterium


Oxalobacter formigenes
Scientific classification edit
Domain: Bacteria
Phylum: Pseudomonadota
Class: Betaproteobacteria
Order: Burkholderiales
Family: Oxalobacteraceae
Genus: Oxalobacter
Species:
O. formigenes
Binomial name
Oxalobacter formigenes
Allison et al, 1985[1]
Type strain
Oxalobacter formigenes OxBT

Oxalobacter formigenes is a Gram negative oxalate-degrading anaerobic bacterium that was first isolated from the gastrointestinal tract of a sheep in 1985.[1] To date, the bacterium has been found to colonize the large intestines of numerous vertebrates, including humans, and has even been isolated from freshwater sediment.[2] It processes oxalate by decarboxylation into formate (oxalyl-CoA decarboxylase), producing energy for itself in the process.[3]

The broad-spectrum quinolone antibiotics kill O. formigenes.[citation needed] If a person's gastrointestinal (GI) tract lacks this bacterium, and therefore lacks the primary source of the oxalyl-CoA decarboxylase enzyme, then the GI tract cannot degrade dietary oxalates; after some vitamin B6-modulated partial metabolic degradation in the body, the oxalates are excreted in the kidney, where they precipitates to form calcium oxalate kidney stones.[4][5][6][7] Oxalobacter formigenes can protect against kidney stones by degrading oxalate.[7]

The role and presence of O. formigenes in the human gut is an area of active research.

Genome

Template:GenomeInfo The genome of O. formigenes has been sequenced by at least three different researchers. It has a G+C content of 49.6%.[8][9]

Taxonomy

Based on fatty acid profile, 16S ribosomal RNA sequencing, and DNA probes specific to the oxc (oxalyl-CoA decarboxylase) gene and frc (formyl-CoA transferase), O. formigenes has been divided into two groups.[1][10][11][12] Group 1 has less diversity and better growth compared to group 2. To date, most research has focused on group 1 strains due to their ease of growth.

Interestingly, analysis with the DNA probes showed that group 2 may be further divided into two subgroups.[11] Whole genome sequencing has revealed that the original O. formigenes taxon can be divided into three additional species: Oxalobacter aliiformigenes, Oxalobacter paeniformigenes, and Oxalobacter paraformigenes.[9]

Growth in culture

O. formigenes was isolated in oxalate containing anerobic media.[1] Currently, O. formigenes is grown in anaerobic Hungate tubes using a CO2-bicarbonate buffered oxalate media.[2] Optimal growth is achieved at a pH between 6 and 7. Oxalate is used at 20 mM for freezer recovery and general maintenance but concentrations can be increased to 100 mM for increased cell density. While oxalate is the main carbon source, small amounts of acetate and yeast extract are supportive of growth.[2] O. formigenes can reach stationary phase in approximately 24 – 48 hours but is sometimes delayed to 72 hours.

Enriched anaerobic complex media (e.g. Brain heart infusion) fail to support the growth of O. formigenes unless supplemented with oxalate. Therefore, these media can be used to assess the purity of O. formigenes cultures.

Antibiotic resistance and susceptibility

Given the fastidious nature of O. formigenes, traditional methods for antibiotic susceptibility testing are not sufficient. Instead, bacteria are cultured in the presence of antibiotics and screened for viability using opaque anaerobic oxalate agar.[2][13][14] This method demonstrated that O. formigenes is resistant to nalidixic acid, ampicillin, amoxicillin, streptomycin, and vancomycin.[13][14] O. formigenes was also found to be susceptible to ciprofloxacin, clarithromycin, clindamycin, doxycycline, gentamicin, levofloxacin, metronidazole, and tetracycline.[13][14]

Prevalence in the mammalian gut

O. formigenes is found in the mammalian gastrointestinal tract and often isolated from feces. In addition to culture-based methods, O. formigenes is presence is detected using molecular methods such as qPCR and next generation sequencing.

Humans

Humans are not typically born with O. formigenes and only become colonized when they begin crawling around in their environment.[15] In adulthood, the frequency of O. formigenes in the gut microbiota varies across different populations. In North India, O. formigenes is prevalent in approximately 65% of the population.[16] In South Korea and Japan, O. formigenes is present in about 75% of individuals.[17][18] In the United States of America, O. formigenes is only detected in about 30% of the human population.[19][20] Populations who do not practice modern medicine or life in a Western lifestyle typically have an increased prevalence of O. formigenes, which could imply that these practices affect O. formigenes colonization.[21][22]

Ruminants

The idea that ruminants are colonized by oxalate-degrading bacteria came from the observation that sheep grazing on oxalate-rich plants (e.g. Halogeton glomeratus) consumed large quantities of this plant and died of renal intoxication from oxalate.[2] However, by slowly acclimatizing sheep to high-oxalate intake, they would survive the consumption of large quantities of oxalate-rich plants.[23] This led to the proposal that resident oxalate-degrading bacteria were enriched by the gradual introduction to a oxalate-rich diet, which protected the sheep from oxalate-induced renal damage.[24][25] In 1980, the first oxalate-degrading bacteria were isolated from the rumen of sheep, and it was later named Oxalobacter formigenes.[1][26]

Potential role in kidney stone disease

O. formigenes has been investigated for its role in mitigating calcium oxalate kidney stone disease because of it metabolizes oxalate as its primary carbon source.

Oxalate degradation

In vitro experiments find that O. formigenes is a specialist oxalate consuming bacteria that can degrade oxalate more efficiently than other generalist oxalate consuming bacteria.[27] Initial research pointed to the loss of oxalate-degrading bacteria, such as O. formigenes, following antibiotic usage as primary contributor to calcium oxalate kidney stone disease.[28][29] Colonization with O. formigenes has been observed to results in a decrease in urinary oxalate[29][4] and reduced frequency of kidney stones[4][7][30]

In a small study, oral supplementation with O. formigenes HC-1 along with a loading dose of oxalate resulted in reduced oxalate excretion during the 6 h immediately following ingestion.[13] However, clinical trials have been unsuccessful in establishing O. formigenes and reducing urinary and plasma concentrations of oxalate.[31][32][33]

Recent work using next-generation sequencing has found that O. formigenes colonizes both calcium oxalate kidney stone formers and non-stone forming controls.[34][35] This observation has led to the notion that O. formigenes alone may not be responsible for regulating oxalate degradation in the gut microbiota, but instead it may be part of a network of co-occurring bacterial taxa that modulate oxalate degradation together.[36][37][38]

Secretagogues to promote intestinal oxalate dumping

It has been proposed that O. formigenes produces secretagogues that can stimulate oxalate transport in epithelial cells. While epithelial oxalate secretion has been shown in human cell lines and rodent models,[39][40] it has not been confirmed in humans. Candidate bioactive molecules have been identified and tested in animal models.[39][41]


References

  1. ↑ 1.0 1.1 1.2 1.3 1.4 "Oxalobacter formigenes gen. nov., sp. nov.: oxalate-degrading anaerobes that inhabit the gastrointestinal tract". Archives of Microbiology 141 (1): 1–7. February 1985. doi:10.1007/BF00446731. PMID 3994481. 
  2. ↑ 2.0 2.1 2.2 2.3 2.4 "Forty Years of Oxalobacter formigenes, a Gutsy Oxalate-Degrading Specialist". Applied and Environmental Microbiology 87 (18): e0054421. August 2021. doi:10.1128/AEM.00544-21. PMID 34190610. Bibcode: 2021ApEnM..87E.544D. 
  3. ↑ "Energy Transduction in Anaerobic Bacteria". Encyclopedia of Biological Chemistry. 2013. pp. 204–209. doi:10.1016/B978-0-12-378630-2.00282-6. ISBN 978-0-12-378631-9. 
  4. ↑ 4.0 4.1 4.2 "Intestinal Oxalobacter formigenes colonization in calcium oxalate stone formers and its relation to urinary oxalate". Journal of Endourology 17 (3): 173–176. April 2003. doi:10.1089/089277903321618743. PMID 12803990. 
  5. ↑ "Can the recurrence of oxalate stones be prevented? Role of Oxalobacter formigenes in stone recurrence.". Journal of Urology 165: S246. 2001. 
  6. ↑ "Medical management of kidney stones: AUA guideline". The Journal of Urology 192 (2): 316–324. August 2014. doi:10.1016/j.juro.2014.05.006. PMID 24857648. 
  7. ↑ 7.0 7.1 7.2 "The role of Oxalobacter formigenes colonization in calcium oxalate stone disease". Kidney International 83 (6): 1144–1149. June 2013. doi:10.1038/ki.2013.104. PMID 23536130. 
  8. ↑ "Genome Sequence of Oxalobacter formigenes Strain OXCC13". Genome Announcements 5 (28): e00534–17. July 2017. doi:10.1128/genomeA.00534-17. PMID 28705966. 
  9. ↑ 9.0 9.1 "New perspectives on an old grouping: The genomic and phenotypic variability of Oxalobacter formigenes and the implications for calcium oxalate stone prevention". Frontiers in Microbiology 13: 1011102. 2022-12-21. doi:10.3389/fmicb.2022.1011102. PMID 36620050. 
  10. ↑ "Studies on the diversity among anaerobic oxalate-degrading bacteria now in the species Oxalobacter formigenes, abstr. I-12". 94th General Meeting of the American Society for Microbiology 1994. Washington, D.C., USA: American Society for Microbiology. 1994. pp. 255. 
  11. ↑ 11.0 11.1 "Identification and classification of Oxalobacter formigenes strains by using oligonucleotide probes and primers". Journal of Clinical Microbiology 35 (2): 350–353. February 1997. doi:10.1128/jcm.35.2.350-353.1997. PMID 9003594. 
  12. ↑ "Class II. Betaproteobacteria class. nov." (in en). Bergey's Manual® of Systematic Bacteriology. Boston, MA: Springer US. 2005. pp. 575–922. doi:10.1007/978-0-387-29298-4_2. ISBN 978-0-387-24145-6. http://link.springer.com/10.1007/0-387-29298-5_2. Retrieved 2022-11-10. 
  13. ↑ 13.0 13.1 13.2 13.3 "Oxalobacter formigenes and its potential role in human health". Applied and Environmental Microbiology 68 (8): 3841–3847. August 2002. doi:10.1128/AEM.68.8.3841-3847.2002. PMID 12147479. Bibcode: 2002ApEnM..68.3841D. 
  14. ↑ 14.0 14.1 14.2 "Sensitivity of human strains of Oxalobacter formigenes to commonly prescribed antibiotics". Urology 79 (6): 1286–1289. June 2012. doi:10.1016/j.urology.2011.11.017. PMID 22656407. 
  15. ↑ "Evaluating Children in the Ukraine for Colonization With the Intestinal Bacterium Oxalobacter formigenes, Using a Polymerase Chain Reaction-based Detection System". Molecular Diagnosis 2 (2): 89–97. June 1997. doi:10.1016/S1084-8592(97)80015-X. PMID 10462596. 
  16. ↑ "Role of Oxalobacter formigenes in calcium oxalate stone disease: a study from North India". European Urology 41 (3): 318–322. March 2002. doi:10.1016/S0302-2838(02)00040-4. PMID 12180235. 
  17. ↑ "Molecular epidemiology of fecal Oxalobacter formigenes in healthy adults living in Seoul, Korea". Journal of Endourology 17 (4): 239–243. May 2003. doi:10.1089/089277903765444384. PMID 12816588. 
  18. ↑ "[Detection of Oxalobacter formigenes in human feces and study of related genes in a new oxalate-degrading bacterium]". Hinyokika Kiyo. Acta Urologica Japonica 49 (7): 371–376. July 2003. PMID 12968475. 
  19. ↑ "The Presence of Oxalobacter formigenes in the Microbiome of Healthy Young Adults". The Journal of Urology 195 (2): 499–506. February 2016. doi:10.1016/j.juro.2015.08.070. PMID 26292041. 
  20. ↑ "Factors related to colonization with Oxalobacter formigenes in U.S. adults". Journal of Endourology 25 (4): 673–679. April 2011. doi:10.1089/end.2010.0462. PMID 21381959. 
  21. ↑ "Comparative prevalence of Oxalobacter formigenes in three human populations". Scientific Reports 9 (1): 574. January 2019. doi:10.1038/s41598-018-36670-z. PMID 30679485. 
  22. ↑ "The microbiome of uncontacted Amerindians". Science Advances 1 (3). April 2015. doi:10.1126/sciadv.1500183. PMID 26229982. 
  23. ↑ "Management practices to minimize death losses of sheep grazing Halogeton-infested range". Journal of Range Management 27 (6): 424–426. November 1974. doi:10.2307/3896714. https://www.jstor.org/stable/3896714. 
  24. ↑ "Changes in ruminal oxalate degradation rates associated with adaptation to oxalate ingestion". Journal of Animal Science 45 (5): 1173–1179. November 1977. doi:10.2527/jas1977.4551173x. PMID 599103. 
  25. ↑ "Enumeration of anaerobic oxalate-degrading bacteria in the ruminal contents of sheep" (in en). FEMS Microbiology Letters 62 (5): 329–334. August 1989. doi:10.1111/j.1574-6968.1989.tb03387.x. 
  26. ↑ "Isolation and some characteristics of anaerobic oxalate-degrading bacteria from the rumen". Applied and Environmental Microbiology 40 (4): 833–839. October 1980. doi:10.1128/aem.40.4.833-839.1980. PMID 7425628. 
  27. ↑ "Characterization and heterologous expression of the oxalyl coenzyme A decarboxylase gene from Bifidobacterium lactis". Applied and Environmental Microbiology 70 (9): 5066–5073. September 2004. doi:10.1128/AEM.70.9.5066-5073.2004. PMID 15345383. 
  28. ↑ "Absence of Oxalobacter formigenes in cystic fibrosis patients: a risk factor for hyperoxaluria". Lancet 352 (9133): 1026–1029. September 1998. doi:10.1016/S0140-6736(98)03038-4. PMID 9759746. 
  29. ↑ 29.0 29.1 "Effect of antibiotics on Oxalobacter formigenes colonization of human gastrointestinal tract". Journal of Endourology 19 (1): 102–106. January 2005. doi:10.1089/end.2005.19.102. PMID 15735393. 
  30. ↑ "Oxalobacter formigenes may reduce the risk of calcium oxalate kidney stones". Journal of the American Society of Nephrology 19 (6): 1197–1203. June 2008. doi:10.1681/ASN.2007101058. PMID 18322162. 
  31. ↑ "Efficacy and safety of Oxalobacter formigenes to reduce urinary oxalate in primary hyperoxaluria". Nephrology, Dialysis, Transplantation 26 (11): 3609–3615. November 2011. doi:10.1093/ndt/gfr107. PMID 21460356. 
  32. ↑ "A randomised Phase I/II trial to evaluate the efficacy and safety of orally administered Oxalobacter formigenes to treat primary hyperoxaluria". Pediatric Nephrology 32 (5): 781–790. May 2017. doi:10.1007/s00467-016-3553-8. PMID 27924398. 
  33. ↑ "A randomised Phase II/III study to evaluate the efficacy and safety of orally administered Oxalobacter formigenes to treat primary hyperoxaluria". Urolithiasis 46 (4): 313–323. August 2018. doi:10.1007/s00240-017-0998-6. PMID 28718073. 
  34. ↑ "16S rRNA gene sequencing reveals altered composition of gut microbiota in individuals with kidney stones". Urolithiasis 46 (6): 503–514. November 2018. doi:10.1007/s00240-018-1037-y. PMID 29353409. 
  35. ↑ "Understanding the gut-kidney axis in nephrolithiasis: an analysis of the gut microbiota composition and functionality of stone formers". Gut 67 (12): 2097–2106. December 2018. doi:10.1136/gutjnl-2017-315734. PMID 29705728. 
  36. ↑ "Gut microbiome and kidney stone disease: not just an Oxalobacter story". Kidney International 96 (1): 25–27. July 2019. doi:10.1016/j.kint.2019.03.020. PMID 31229040. 
  37. ↑ "Inhibition of urinary stone disease by a multi-species bacterial network ensures healthy oxalate homeostasis". Kidney International 96 (1): 180–188. July 2019. doi:10.1016/j.kint.2019.02.012. PMID 31130222. 
  38. ↑ "Oxalobacter formigenes-associated host features and microbial community structures examined using the American Gut Project". Microbiome 5 (1): 108. August 2017. doi:10.1186/s40168-017-0316-0. PMID 28841836. 
  39. ↑ 39.0 39.1 "Oxalobacter formigenes-Derived Bioactive Factors Stimulate Oxalate Transport by Intestinal Epithelial Cells". Journal of the American Society of Nephrology 28 (3): 876–887. March 2017. doi:10.1681/ASN.2016020132. PMID 27738124. 
  40. ↑ "Oxalobacter sp. reduces urinary oxalate excretion by promoting enteric oxalate secretion". Kidney International 69 (4): 691–698. February 2006. doi:10.1038/sj.ki.5000162. PMID 16518326. 
  41. ↑ "Sel1-like proteins and peptides are the major Oxalobacter formigenes-derived factors stimulating oxalate transport by human intestinal epithelial cells". American Journal of Physiology. Cell Physiology 325 (1): C344–C361. July 2023. doi:10.1152/ajpcell.00466.2021. PMID 37125773. 

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