Oxalate consumption by lactobacilli: evaluation of oxalyl-CoA decarboxylase and formyl-CoA transferase activity in Lactobacillus acidophilus

Turroni, Silvia; Vitali, Beatrice; Bendazzoli, Claudia; Candela, Marco; Gotti, Roberto; Federici, Federica; Pirovano, F.; Brigidi, Patrizia

doi:10.1111/j.1365-2672.2007.03388.x

Cited by 99 publications

(100 citation statements)

References 42 publications

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“…Previous studies have implicated the Lactobacillus genus as a potentially important contributor to oxalate degradation in the mammalian gut (34,51). The results of this study suggest that lactobacilli are the primary oxalate-degrading bacteria present in N. albigula.…”

Section: Discussionsupporting

confidence: 57%

“…One of the best-studied species is Oxalobacter formigenes, which requires oxalate as a carbon and energy source for growth (8). However, other oxalate-degrading bacteria include species from the genera Lactobacillus, Bifidobacterium, Streptococcus, Enterococcus, and others (11,(32)(33)(34)(35). The majority of studies investigating oxalate-degrading bacteria have been conducted on humans, lab rats, and agricultural systems.…”

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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: Discussionsupporting

confidence: 57%

mentioning

confidence: 99%

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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“…Although E. coli has been implicated in the biomineralization processes leading to the formation of calcium oxalate crystals (10), recent measurements suggest that E. coli does not degrade oxalate in media containing this compound at a 5 mM concentration (57). The experiments, however, did not systematically vary the incubation conditions, and so it is possible that conditions under which E. coli can metabolize exogenous oxalate exist.…”

Section: Discussionmentioning

confidence: 87%

Differential Substrate Specificity and Kinetic Behavior of Escherichia coli YfdW and Oxalobacter formigenes Formyl Coenzyme A Transferase

et al. 2008

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The yfdXWUVE operon appears to encode proteins that enhance the ability of Escherichia coli MG1655 to survive under acidic conditions. Although the molecular mechanisms underlying this phenotypic behavior remain to be elucidated, findings from structural genomic studies have shown that the structure of YfdW, the protein encoded by the yfdW gene, is homologous to that of the enzyme that mediates oxalate catabolism in the obligate anaerobe Oxalobacter formigenes, O. formigenes formyl coenzyme A transferase (FRC). We now report the first detailed examination of the steady-state kinetic behavior and substrate specificity of recombinant, wild-type YfdW. Our studies confirm that YfdW is a formyl coenzyme A (formyl-CoA) transferase, and YfdW appears to be more stringent than the corresponding enzyme (FRC) in Oxalobacter in employing formyl-CoA and oxalate as substrates. We also report the effects of replacing Trp-48 in the FRC active site with the glutamine residue that occupies an equivalent position in the E. coli protein. The results of these experiments show that Trp-48 precludes oxalate binding to a site that mediates substrate inhibition for YfdW. In addition, the replacement of Trp-48 by Gln-48 yields an FRC variant for which oxalate-dependent substrate inhibition is modified to resemble that seen for YfdW. Our findings illustrate the utility of structural homology in assigning enzyme function and raise the question of whether oxalate catabolism takes place in E. coli upon the up-regulation of the yfdXWUVE operon under acidic conditions.With the completion of genome sequences for several strains of Escherichia coli (6,27,45,61), attention has turned to the annotation of proteins encoded by specific genes of unknown function (56). Deletion studies have shown that the yfdXWUVE operon, in which the yfdX gene is under the control of the EvgAS regulatory system (40), encodes proteins that enhance the ability of E. coli MG1655 to survive under acidic conditions (41). Although the molecular mechanisms underlying this phenotypic behavior remain to be elucidated, the proteins encoded by the yfdW and yfdU genes in this operon (YfdW and YfdU, respectively) are homologous to proteins present in the obligate anaerobe Oxalobacter formigenes (53), O. formigenes formyl coenzyme A transferase (FRC) (2, 30, 46) and oxalyl coenzyme A (oxalyl-CoA) decarboxylase (3, 5). We note that FRC and oxalyl-CoA decarboxylase are essential for the survival of Oxalobacter in that they mediate the conversion of oxalate into formate and CO 2 in a coupled catalytic cycle (Fig. 1). In combination with an oxalate-formate antiporter (OxlT) (29, 60), this cycle is thought to maintain the electrochemical and pH gradients needed for ATP synthesis (1, 35). It has therefore been proposed previously that (i) YfdW catalyzes the conversion of oxalate into oxalyl-CoA by using formyl-CoA as a donor and (ii) the YfdU protein mediates oxalyl-CoA decarboxylation (26). High-resolution X-ray crystallography supports the likely functional similarity of FRC and YfdW...

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“…Oxalate is not a substrate for liposomes reconstituted from endogenous E. coli XL3 proteins grown in LB at pH 7 (58), nor is it metabolized by E. coli under conditions in which activity is seen in Lactobacillus species (40). We hypothesized that YfdW and YfdU are part of an AR2-like system where oxalate is brought into the cell by YhjX and decarboxylated in a reaction similar to that catalyzed by GadA/B in the challenge medium.…”

mentioning

confidence: 99%

“…Oxalate in mammals results from dietary sources, like rhubarb and spinach, and as a by-product of amino acid degradation (39). Humans have no endogenous oxalate metabolism, but bacteria such as Lactobacillus acidophilus (40), Bifidobacterium animalis (35), and Oxalobacter formigenes (41,42) are believed to metabolize oxalate in the human gut (43).…”

mentioning

confidence: 99%

YfdW and YfdU Are Required for Oxalate-Induced Acid Tolerance in Escherichia coli K-12

et al. 2013

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Escherichia coli has several mechanisms for surviving low-pH stress. We report that oxalic acid, a small-chain organic acid (SCOA), induces a moderate acid tolerance response (ATR) in two ways. Adaptation of E. coli K-12 at pH 5.5 with 50 mM oxalate and inclusion of 25 mM oxalate in pH 3.0 minimal challenge medium separately conferred protection, with 67% ؎ 7% and 87% ؎ 17% survival after 2 h, respectively. The combination of oxalate adaptation and oxalate supplementation in the challenge medium resulted in increased survival over adaptation or oxalate in the challenge medium alone. The enzymes YfdW, a formyl coenzyme A (CoA) transferase, and YfdU, an oxalyl-CoA decarboxylase, are required for the adaptation effect but not during challenge. Unlike other SCOAs, this oxalate ATR is not a part of the RpoS regulon but appears to be linked to the signal protein GadE. We theorize that this oxalate ATR could enhance the pathogenesis of virulent E. coli consumed with oxalate-containing foods like spinach.

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Oxalate consumption by lactobacilli: evaluation of oxalyl-CoA decarboxylase and formyl-CoA transferase activity in Lactobacillus acidophilus

Cited by 99 publications

References 42 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

Differential Substrate Specificity and Kinetic Behavior of Escherichia coli YfdW and Oxalobacter formigenes Formyl Coenzyme A Transferase

YfdW and YfdU Are Required for Oxalate-Induced Acid Tolerance in Escherichia coli K-12

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