Prevotella: A Key Player in Ruminal Metabolism

Abstract

Ruminants are foregut fermenters that have the remarkable ability of converting plant polymers that are indigestible to humans into assimilable comestibles like meat and milk, which are cornerstones of human nutrition. Ruminants establish a symbiotic relationship with their microbiome, and the latter is the workhorse of carbohydrate fermentation. On the other hand, during carbohydrate fermentation, synthesis of propionate sequesters H, thus reducing its availability for the ultimate production of methane (CH4) by methanogenic archaea. Biochemically, methane is the simplest alkane and represents a downturn in energetic efficiency in ruminants; environmentally, it constitutes a potent greenhouse gas that negatively affects climate change. Prevotella is a very versatile microbe capable of processing a wide range of proteins and polysaccharides, and one of its fermentation products is propionate, a trait that appears conspicuous in P. ruminicola strain 23. Since propionate, but not acetate or butyrate, constitutes an H sink, propionate-producing microbes have the potential to reduce methane production. Accordingly, numerous studies suggest that members of the genus Prevotella have the ability to divert the hydrogen flow in glycolysis away from methanogenesis and in favor of propionic acid production. Intended for a broad audience in microbiology, our review summarizes the biochemistry of carbohydrate fermentation and subsequently discusses the evidence supporting the essential role of Prevotella in lignocellulose processing and its association with reduced methane emissions. We hope this article will serve as an introduction to novice Prevotella researchers and as an update to others more conversant with the topic.

Keywords: Prevotella; carbohydrate metabolism; methane emissions; propionate; sustainable agriculture.

Figure 1

Ruminal carbohydrates fermentation. (A) Ruminants lack enzymes for digestion of cellulose contained in the cell wall of plant material. Therefore, digestion of carbohydrates starts with initial mastication and passage of feedstuff to the rumen (green arrow), where cellulolytic bacteria partially degrade plant cell walls. Semi-digested material flows then to the reticulum, which facilitates regurgitation (red arrow) and rechewing of feed particles. Remasticated, finer feed particles are mobilized to the omasum (blue arrow). Finally, feedstuff passes to the abomasum (black arrow), which is considered the true stomach where an acidic pH facilitates digestion of microbial and plant proteins. (B) Simplified schematics of carbohydrate fermentation. (i) Breakdown of polysaccharides to monosaccharides; (ii) A glucose molecule is oxidized into two molecules of pyruvate with concomitant reduction of NAD⁺ to NADH; (iii) Pentose metabolism through the pentose cycle and transketolase cleavage; (iv) Pyruvate oxidative decarboxylation with production of CO₂, reduced ferredoxin and acetyl-CoA. An alternative reaction releases formate instead CO₂ and reduced ferredoxin; (v) Acetate production; (vi) Butyrate production; (vii) Propionate production via the succinate pathway; (viii) Propionate production via acrylate pathway. (ix) Interspecies hydrogen transference; (x) Production of molecular hydrogen through electron confurcation; (xi) Hydrogenotrophic methanogenesis; (xii) Reductive acetogenesis; which is a smaller H₂ sink than (xi). Not all reactants or products are shown. Figure 1B was modified from [85]. Orange thick arrows indicate points where the redox couple (NAD+ and NADH) promote chemical reactions. (C) Genetic architectures of some PUL loci in P. copri, the central SusC/D proteins, the hybrid two component system (HTCS), glycoside hydrolases (GH), pectate lyases (PL) and surface glycan binding proteins (SGBP) are depicted. Figure 1C was modified from [86].

Figure 2

Inverse correlation between Prevotella abundance and methane emissions. Data from Aguilar-Marin et al., 2020 [36]. Results from linear discriminant analysis with software LEfSe. All presented results had a p-value < 0.05 and showed that many species of Prevotella (left panel) or proteins from Prevotella (right panel) were more abundant in animals that exhibited lower methane emissions (green bars). Red bars depict taxa or proteins that were more abundant in animals with high methane emissions. P: Prevotella. Suffixes A, B, C and D in Prevotella ruminicola species are arbitrary and are used here only to denote that four different strains of such a species were found differentially accumulated. For the sake of space, names of proteins in the right panel were arbitrarily abbreviated. All green bars correspond to Prevotella proteins while the two red bars correspond to proteins from Bacteroides ovatus (DNA gyrase, top bar) and [Ruminoccocacea bacterium AB4001] (Oxoloacetate decarboxylase). Full names of proteins can be found in Figure 6 of Aguilar-Marin et al., 2022 [36].