The Rumen - a fermentation vat or a series of organized structured microbial consortia: implications for the mitigation of enteric methane production by feed additives

Abstract

The rumen has been viewed as a fermentation vat with free floating (planktonic) microbes, particle associated microbes and microbes that attach to the epithelial cells of the rumen wall. The rumen is described, in general, as a, anaerobic microbial ecosystem containing a milieu of bacteria, archaea, protozoa, bacteriophage and phycomycetous fungi that degrade organic matter with the ultimate production of volatile fatty acids (VFA), the energy that becomes available is used for maintenance and growth of cells. The VFA are absorbed from the upper part of the digestive tract and the microbial cells provide essential nutrients such as amino acids, when they are digested by intestinal enzymes on wash out from the rumen. Since about 1980 there has been an emerging realization that possibly as high as 80-90% of the rumen microbial biomass is present as associated and interactive colonies in biofilms on both inert and insoluble organic matter in the rumen and that the planktonic cells play little role in feed digestion. Biofilms consist of microbial cells and a wide range of self-generated extra- cellular polymeric substances. Biofilm formation is a dynamic process, which is coordinated by the interactions of different microbial species. These biofilms that form within a few minutes of feed being immersed in rumen fluid, provide spatially separated microbial colonies held in an extracellular polymeric substance (EPS), including polysaccharides, nucleic acids, and proteins that is progressively produced by the microbes as they position themselves in the biofilm. The sequential deposition and growth of sessile microbes within the biofilm matrix allows the nutrients produced as end products of one species to be efficiently transferred to other species which use these as substrate for energy metabolism. The overall conversion of plant organic matter to VFA in the biofilm results in the production of reduced cofactors which revert to their oxidized form by releasing the electron as hydrogen. This depends on the maintenance of a low concentration of hydrogen and requires rapid uptake of hydrogen by microbes that can use high affinity electron acceptors such as nitrate, sulphate and carbon dioxide. Methanogenic Archae which obtain energy by reducing carbon dioxide are mainly responsible, but sulphur reducing bacteria also play a minor role in the rumen. The requirements for minimal concentrations of hydrogen in the culture medium demand that the syntrophic microbes are closely associated. Syntrophism is a special case of symbiotic cooperation between two metabolically different types of bacteria which depend on each other for degradation of a certain substrate, typically for energetic reasons. Biofilm formation on feed particulate matter is essential for efficient fermentative digestion in the rumen, as it provides the ecological niche that ensures that the syntrophic organisms involved are spatially aligned to ensure efficient capture of hydrogen to prevent feed back inhibition of the reactions involved in converting polymeric feed materials to their end products. The overall conclusion pertinent to this symposium is that because of the need for symbiotic associations in biofilm microbial colonies on feed particles in the rumen, it is not logical to attempt to lower methane production by including chemicals in a diet that specifically target the inhibition of methanogens, unless alternative electron sinks are provided. Where compounds that can be used by microbes as electron sinks are included in the culture media , the organism using these as sources of energy must also be spatially distributed in the biofilm to maintain hydrogen concentrations at a minimum for the efficient oxidation of reduced cofactors generated in the reactions occurring in fermentation. Nitrate reducing and sulphur reducing bacteria appear to full fill this role highly efficiently.