Impact of oxalic acid on rumen function and bacterial community in sheep

Abstract

Oxalic acid (OA) is a secondary compound occurring in a wide range of plants consumed by ruminants, especially in saline lands or in arid and semi-arid regions. However, its impact on the rumen microbial community and its changes over time, as well as the potential consequences on ruminal function, remain unknown. To examine this impact, five ewes fitted with a ruminal cannula and fed low-quality grass hay were dosed daily with 0.6 mmol of OA/kg body weight through the cannula for 14 days. On days 0 (before the start), 4, 7 and 14 of the administration period, samples of ruminal digesta were collected throughout the day (0, 3, 6 and 9 h after the morning feeding) for analysis of the bacterial community and fermentation parameters (pH, ammonia and volatile fatty acid (VFA) concentrations). In addition, two feedstuffs were incubated in situ using the nylon bag technique to estimate ruminal degradation. Terminal restriction fragment length polymorphism was employed to monitor the dynamics of total bacteria, and quantitative real-time PCR was used to investigate the abundance of the oxalate-degrading Oxalobacter formigenes. Neither pH nor total VFA concentrations were affected. Nevertheless, OA dosing altered molar proportions of most individual VFA and ammonia concentrations ( P , 0.001). The dry matter disappearance of alfalfa hay was reduced on days 7 and 14 and that of barley straw only on day 7 ( P , 0.01). These slight changes were related to others observed in the relative frequency of a number of terminal restriction fragments. Variations in the ruminal microbiota occurred rapidly with OA administration, which did not modify the bacterial diversity significantly but altered the structure of the community. However, many of these changes were reversed by the end of the experiment, with no significant differences between days 0 and 14 of dosing. These results suggest a rapid adaptation of the rumen bacterial community linked to the estimated increase in the abundance of O. formigenes (from 0.002% to 0.007% of oxc gene in relation to the total bacteria 16S rDNA; P , 0.01), which is assumed to be responsible for oxalate breakdown.

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

“…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). In the current study, organisms in fecal samples were among the least representative of Oxalobacter abundances across the gut.…”

“…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.…”

“…We have shown that consortia of oxalate-degrading bacteria are present and distributed throughout the gut in mammalian herbivores that specialize on oxalate-rich plants, with fecal communities being among the least representative of potential oxalate-degrading bacteria. The oxalate-degrading function of the gut microbiota may be the result of a responsive community (54). Complex ecological interactions between host, diet, and microbiota can have considerable impacts on the composition and function of the microbiota and, subsequently, the host phenotype.…”

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

“…Second, there is a need to understand how oxalate affects the mammalian gut microbiota as a whole. Previous research has focused on the role of individual taxa in oxalate degradation (7,20,29,37,38). However, several oxalate-degrading taxa have now been identified from the mammalian gut, and other taxa may be affected by oxalate in obscure ways (20,26,39,40).…”

“…To examine the interactions between dietary oxalate and gut microbes, animals were placed in a diet trial where oxalate was gradually increased over time ( Table 1). The 5-day time periods for the 0.05% oxalate diet were chosen to ensure that any effect of oxalate on the microbiota was removed, while a 3-day period for each of the oxalate diet periods was chosen based on the study of Belenguer et al (29), in which 3 days on oxalate was long enough to elicit a microbial response. Metabolic cages were used to separate urine and feces and allow for the quantification of food and water intake, which were given ad libitum.…”