Microbial degradation of oxalate in the gastrointestinal tracts of rodents and ruminants

Daniel, Steven L.

doi:10.31274/rtd-180813-12873

Cited by 13 publications

(18 citation statements)

References 175 publications

(179 reference statements)

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“…Some genera, such as Lactobacillus, Clostridium, and Enterococcus, exhibit relatively low rates of oxalate degradation (0 to 7 mol/ml medium/day), whereas others, such as Providencia, Oxalophagus, and Oxalobacter, have much higher rates (20 to 400 mol/ml medium/day). Furthermore, the oxalate-degrading rates of whole communities, as well as the proportion of oxalatedegrading bacteria comprising a community, fluctuate with oxalate concentrations in the immediate environment (41,54). Thus, oxalate in the immediate environment of microbial communities may drive the oxalate-degrading function in the short term to respond to dynamic concentrations of oxalate.…”

Section: Discussionmentioning

confidence: 99%

“…In humans, there are ϳ1 million Oxalobacter cells/g (24). Rats harbor ϳ10 million Oxalobacter cells/g, or Ͻ0.1% of the community (41). In sheep, Oxalobacter makes up ϳ0.007% of the community in the rumen (54).…”

Section: Discussionmentioning

confidence: 99%

“…To isolate oxalate-tolerant and oxalatedegrading bacteria, serial dilutions of gut contents were plated onto brain heart infusion (BHI) agar supplemented with 20 mM sodium oxalate and 1 g/liter calcium chloride. The addition of sodium oxalate and calcium chloride produces calcium oxalate precipitate, which can be used to determine if bacteria are degrading oxalate (8,41). The genus Lactobacillus is dominant in other woodrat species and contains numerous toxin-degrading species (2,42,43).…”

Section: Methodsmentioning

confidence: 99%

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The Gastrointestinal Tract of the White-Throated Woodrat (Neotoma albigula) Harbors Distinct Consortia of Oxalate-Degrading Bacteria

Miller

Kohl

Dearing

2014

Appl Environ Microbiol

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The microbiota inhabiting the mammalian gut is a functional organ that provides a number of services for the host. One factor that may regulate the composition and function of gut microbial communities is dietary toxins. Oxalate is a toxic plant secondary compound (PSC) produced in all major taxa of vascular plants and is consumed by a variety of animals. The mammalian herbivore Neotoma albigula is capable of consuming and degrading large quantities of dietary oxalate. We isolated and characterized oxalate-degrading bacteria from the gut contents of wild-caught animals and used high-throughput sequencing to determine the distribution of potential oxalate-degrading taxa along the gastrointestinal tract. Isolates spanned three genera: Lactobacillus, Clostridium, and Enterococcus. Over half of the isolates exhibited significant oxalate degradation in vitro, and all Lactobacillus isolates contained the oxc gene, one of the genes responsible for oxalate degradation. Although diverse potential oxalate-degrading genera were distributed throughout the gastrointestinal tract, they were most concentrated in the foregut, where dietary oxalate first enters the gastrointestinal tract. We hypothesize that unique environmental conditions present in each gut region provide diverse niches that select for particular functional taxa and communities.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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The Gastrointestinal Tract of the White-Throated Woodrat (Neotoma albigula) Harbors Distinct Consortia of Oxalate-Degrading Bacteria

Miller

Kohl

Dearing

2014

Appl Environ Microbiol

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“…In previous studies in rats (4,15,25), it was demonstrated that the success and maintenance of colonization depend on the availability of intraluminal oxalate and, in particular, the balance between intraluminal oxalate and calcium (15). In the present study, we have shown that Agxt and WT mice are readily colonized by esophageal gavage of a live rat strain of Oxalobacter cells, but there was a striking difference between the two groups in terms of the duration of colonization after the oxalate-supplemented diet (0.5% calcium) was replaced by regular chow (1% calcium).…”

Section: Discussionmentioning

confidence: 99%

Enteric oxalate elimination is induced and oxalate is normalized in a mouse model of primary hyperoxaluria following intestinal colonization withOxalobacter

Hatch

Gjymishka

Salido

et al. 2011

American Journal of Physiology-Gastrointestinal and Liver Physi

130

143

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Hatch M, Gjymishka A, Salido EC, Allison MJ, Freel RW. 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, 2011. First published December 16, 2010; doi:10.1152/ajpgi.00434.2010.-Oxalobacter colonization of rat intestine was previously shown to promote enteric oxalate secretion and elimination, leading to significant reductions in urinary oxalate excretion (Hatch et al. Kidney Int 69: 691-698, 2006). The main goal of the present study, using a mouse model of primary hyperoxaluria type 1 (PH1), was to test the hypothesis that colonization of the mouse gut by Oxalobacter formigenes could enhance enteric oxalate secretion and effectively reduce the hyperoxaluria associated with this genetic disease. Wild-type (WT) mice and mice deficient in liver alanine-glyoxylate aminotransferase (Agxt) exhibiting hyperoxalemia and hyperoxaluria were used in these studies. We compared the unidirectional and net fluxes of oxalate across isolated, short-circuited large intestine of artificially colonized and noncolonized mice. In addition, plasma and urinary oxalate was determined. Our results demonstrate that the cecum and distal colon contribute significantly to enteric oxalate excretion in Oxalobacter-colonized Agxt and WT mice. In colonized Agxt mice, urinary oxalate excretion was reduced 50% (to within the normal range observed for WT mice). Moreover, plasma oxalate concentrations in Agxt mice were also normalized (reduced 50%). Colonization of WT mice was also associated with marked (up to 95%) reductions in urinary oxalate excretion. We conclude that segment-specific effects of Oxalobacter on intestinal oxalate transport in the PH1 mouse model are associated with a normalization of plasma oxalate and urinary oxalate excretion in otherwise hyperoxalemic and hyperoxaluric animals. cecum; proximal colon; distal colon; slc26a6 CONSIDERABLE EVIDENCE HAS emerged from human and animal studies suggesting that colonization of the intestinal tract by the anaerobic bacterium Oxalobacter formigenes plays an important role in degrading dietary sources of oxalate in the intestine, leading to reduced intestinal oxalate absorption and, consequently, a lower urinary oxalate excretion (9, 10, 15, 18 -20, 22, 25-27, 29). Importantly, these bacteria, discovered by Allison et al.(1) in 1985, use oxalate as a sole carbon and energy source. In most of the studies involving human subjects, the approach has been to determine whether the lack of Oxalobacter colonization is associated with increased urinary oxalate excretion and stone formation (9, 10, 18 -20, 22, 26, 29). Clinical findings suggest a direct correlation between the complete absence or decreased activity of luminal Oxalobacter and the development of recurrent oxalate stone disease (18), as well as the hyperoxaluria associated with conditions such as inflammatory bowel disease, jejunoileal bypass, and cystic fibrosis (9,10,2...

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“…Strain Va3 (Rowett Research Institute culture collection) was isolated by enrichment of the feces from an adult volunteer. The medium used was medium D2, which is medium D of Daniel et al (11), modified by replacing the trace elements listed in reference 11 with those listed in reference 23. The main components were as follows (amounts are liter Ϫ1 ): di-sodium oxalate, 2.68 g; clarified rumen fluid, 200 ml; sodium acetate ⅐ 3H 2 O, 1.36 g; yeast extract (Difco), 1 g; minerals; and 1 g of cysteine HCl as a reductant.…”

Section: Methodsmentioning

confidence: 99%

Oxalobacter formigenes and Its Potential Role in Human Health

Duncan¹,

Richardson²,

Kaul³

et al. 2002

Appl Environ Microbiol

166

123

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Oxalate degradation by the anaerobic bacterium Oxalobacter formigenes is important for human health, helping to prevent hyperoxaluria and disorders such as the development of kidney stones. Oxalate-degrading activity cannot be detected in the gut flora of some individuals, possibly because Oxalobacter is susceptible to commonly used antimicrobials. Here, clarithromycin, doxycycline, and some other antibiotics inhibited oxalate degradation by two human strains of O. formigenes. These strains varied in their response to gut environmental factors, including exposure to gastric acidity and bile salts. O. formigenes strains established oxalate breakdown in fermentors which were preinoculated with fecal bacteria from individuals lacking oxalate-degrading activity. Reducing the concentration of oxalate in the medium reduced the numbers of O. formigenes bacteria. Oxalate degradation was established and maintained at dilution rates comparable to colonic transit times in healthy individuals. A single oral ingestion of O. formigenes by adult volunteers was, for the first time, shown to result in (i) reduced urinary oxalate excretion following administration of an oxalate load, (ii) the recovery of oxalate-degrading activity in feces, and (iii) prolonged retention of colonization.Oxalate is formed in the liver by amino acid catabolism (18). It is also present in a wide range of food and drinks, including tea, coffee, chocolate, and fruit and vegetables (19). The concentration of oxalate voided in the urine plays an important role in urolithiasis, the formation of calcium oxalate kidney stones (27). The main known bacterial species involved in oxalate degradation in the gut is the anaerobe Oxalobacter formigenes. First isolated from ruminants (13), O. formigenes has been found in many animal species and in humans (reviewed by Allison et al. [3]). Almost all 6-to 8-year-old individuals tested possess O. formigenes, but this bacterium may later be lost and it is detected in the feces of 60 to 80% of adults (31). The therapeutic use of antibiotics and other drugs may contribute to the loss of O. formigenes (6; M. J. Allison, H. Sidhu, and A. B. Peck, Abstr. 22nd Int. Cong. Microb. Ecol. Dis., abstr. 5.002, 1997). Patients with cystic fibrosis often lack fecal oxalate degraders, perhaps because of intensive drug therapy (32).Understanding the ecology of O. formigenes could aid our knowledge of oxalate metabolism in the gut. This might lead to the use of probiotics to combat hyperoxaluria. Here we describe experiments performed in vitro and in vivo which aimed to measure relevant physiological properties of O. formigenes and the consequences of its introduction in fermentors simulating conditions in the human colon and in human volunteers. State University) were isolated from sheep rumen (13) and human feces (2), respectively. Strain Va3 (Rowett Research Institute culture collection) was isolated by enrichment of the feces from an adult volunteer. The medium used was medium D2, which is medium D of Daniel et al. (11), modified by...

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Microbial degradation of oxalate in the gastrointestinal tracts of rodents and ruminants

Cited by 13 publications

References 175 publications

The Gastrointestinal Tract of the White-Throated Woodrat (Neotoma albigula) Harbors Distinct Consortia of Oxalate-Degrading Bacteria

The Gastrointestinal Tract of the White-Throated Woodrat (Neotoma albigula) Harbors Distinct Consortia of Oxalate-Degrading Bacteria

Enteric oxalate elimination is induced and oxalate is normalized in a mouse model of primary hyperoxaluria following intestinal colonization withOxalobacter

Oxalobacter formigenes and Its Potential Role in Human Health

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