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

Abstract

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.

Effect of Dietary Oxalate on the Gut Microbiota of the Mammalian Herbivore Neotoma albigula

“…Of these OTU, 97.6% were assigned to 14 bacterial phyla with 25.3% assigned to 88 genera. The fecal microbiota showed a composition typical of woodrats and other mammals that was dominated by Bacteroidetes, particularly the family S24-7 that comprised between 49.8 to 67.2% of the microbiota (26). There were no significant differences in community membership or community structure across treatments, based on the ANOSIM (P ϭ 0.496 and 0.691, respectively) (Fig.…”

“…Additionally, the by-products of microbial oxalate degradation, formate and CO 2 , may be used by a number of bacteria in the process of acetogenesis or methanogenesis, potentially benefitting other gut bacteria not directly involved in the oxalate degradation function (23). While there is no direct evidence for either acetogenesis or methanogenesis, several known acetogenic taxa, such as Clostridium, Streptococcus, and Ruminococcus, are prevalent in the N. albigula gut (24)(25)(26). These attributes constitute a unique system to isolate the interactions between dietary toxins and gut microbes, along with their contribution to the overall metabolism of the host.…”

“…This high level of oxalate degradation has been hypothesized to be the result of microbial metabolism (27,28). Furthermore, N. albigula harbors a diversity of known and potentially oxalate-degrading bacteria distributed across the gastrointestinal tract, including Oxalobacter, Lactobacillus, Clostridium, and Enterococcus, among others (26). Thus, N. albigula regularly consumes large amounts of oxalate and harbors a diversity of bacteria that exhibit complex interactions with oxalate, making it an ideal species to elucidate oxalate-microbiota interactions.…”

“…Some populations of N. albigula consume a diet composed of nearly 100% Opuntia species cactus, which contains a high oxalate content (1.5%, dry weight) (26). Neotoma albigula can degrade Ͼ90% of dietary oxalate when fed artificial diets of up to 9% oxalate (dry weight).…”

Probiotics for prevention of urinary stones

“…Along these lines, recent studies in the white-throated wood rat Neotoma albigula are of interest (39). This mammal consumes a diet comprised almost entirely of the oxalate-rich Opuntia cactus.…”