Unravelling methanogenesis in ruminants, horses and kangaroos: the links between gut anatomy, microbial biofilms and host immunity

Abstract

The present essay aims to resolve the question as to why macropod marsupials (e.g. kangaroos and wallabies, hereinafter termed ‘macropods) and horses produce much less methane (CH4) than do ruminants when digesting the same feed. In herbivores, gases produced during fermentation of fibrous feeds do not pose a major problem in regions of the gut that have mechanisms to eliminate them (e.g. eructation in the rumen and flatus in the lower bowel). In contrast, gas pressure build-up in the tubiform forestomach of macropods or in the enlarged tubiform caecum of equids would be potentially damaging. It is hypothesised that, to prevent this problem, evolution has favoured development of controls over gut microbiota that enable enteric gas production (H2 and CH4) to be differently regulated in the forestomach of macropods and the caecum of all three species, from the forestomach of ruminants. The hypothesised regulation depends on interactions between their gut anatomy and host-tissue immune responses that have evolved to modify the species composition of their gut microbiota which, importantly, are mainly in biofilms. Obligatory H2 production during forage fermentation is, thus, captured in CH4 in the ruminant where ruminal gases are readily released by eructation, or in acetate in the macropod forestomach and equid caecum–colon where a build-up in gas pressure could potentially damage these organs. So as to maintain appropriate gut microbiota in different species, it is hypothesised that blind sacs at the cranial end of the haustral anatomy of the macropod forestomach and the equid caecum are sites of release of protobiofilm particles that develop in close association with the mucosal lymphoid tissues. These tissues release immune secretions such as antimicrobial peptides, immunoglobulins, innate lymphoid cells and mucin that eliminate or suppress methanogenic Archaea and support the growth of acetogenic microbiota. The present review draws on microbiological studies of the mammalian gut as well as other microbial environments. Hypotheses are advanced to account for published findings relating to the gut anatomy of herbivores and humans, the kinetics of digesta in ruminants, macropods and equids, and also the composition of biofilm microbiota in the human gut as well as aquatic and other environments where the microbiota exist in biofilms.