Interactions between microbial consortia in biofilms: a paradigm shift in rumen microbial ecology and enteric methane mitigation

Minimising enteric CH4 emissions from ruminants is a current research priority because CH4 contributes to global warming. The most effective mitigation strategy is to adjust the animal's diet to complement locally available feed resources so that optimal production is gained from a minimum of animals. This essay concentrates on a second strategy - the use of feed additives that are toxic to methanogens or that redirect H-2 (and electrons) to inhibit enteric CH4 emissions from individual animals. Much of the published research in this area is contradictory and may be explained when the microbial ecology of the rumen is considered. Rumen microbes mostly exist in organised consortia within biofilms composed of self-secreted extracellular polymeric substances attached to or within feed particles. In these biofilms, individual colonies are positioned to optimise their use of preferred intermediates from an overall process of organic matter fermentation that generates end-products the animal can utilise. Synthesis of CH4 within biofilms prevents a rise in the partial pressure of H-2 (pH(2)) to levels that inhibit bacterial dehydrogenases, and so reduce fermentation rate, feed intake and digestibility. In this context, hypotheses are advanced to explain changes in hydrogen disposal from the biofilms in the rumen resulting from use of anti-methanogenic feed additives as follows. Nitrate acts as an alternative electron sink when it is reduced via NO2- to NH3 and CH4 synthesis is reduced. However, efficiency of CH4 mitigation is always lower than that predicted and decreases as NO3- ingestion increases. Suggested reasons include (1) variable levels of absorption of NO3- or NO2- from the rumen and (2) increases in H-2 production. One suggestion is that NO3- reduction may lower pH(2) at the surface of biofilms, thereby creating an ecological niche for growth of syntrophic bacteria that oxidise propionate and/or butyrate to acetate with release of H-2. Chlorinated hydrocarbons also inhibit CH4 synthesis and increase H-2 and formate production by some rumen methanogens. Formate diffuses from the biofilm and is converted to HCO3- and H-2 in rumen fluid and is then excreted via the breath. Short-chain nitro-compounds inhibit both CH4 and formate synthesis when added to ruminal fluid but have little or no effect in redirecting H-2 to other sinks, so the pH(2) within biofilms may increase to levels that support reductive acetogenesis. Biochar or activated charcoal may also alter biofilm activity and reduce net CH4 synthesis; direct electron transfer between microbes within biofilms may also be involved. A final suggestion is that, during their sessile life stage, protozoa interact with biofilm communities and help maintain pH(2) in the biofilm, supporting methanogenesis.