The dynamic gut: the vertebrate gastrointestinal tract and associated microbiome exhibit physiological flexibility and adaptations to diet

Abstract

In this Review, we consider evidence for the adaptive digestionhypothesis (ADH), which proposes that digestive enzyme andtransporter levels should usually relate positively to levels of theirrespective dietary substrates. In this way, energy is not wasted inmaintaining the molecular machinery needed to hydrolyze andabsorb substrates that are present at low levels. Genomic,transcriptomic and functional studies generally support this notion,as observed from evolutionary transitions to starch-rich diets in avianand mammalian lineages, and comparative studies in mammals,birds and fish specializing on different diets (e.g. plants, flesh, fruit,nectar, insects). Furthermore, studies of vertebrates’ microbiomesprovide evidence of large-scale shifts in microbial taxonomy andfunction in accordance with the specialized dietary strategies of hostsacross evolutionary time scales. Omnivorous vertebrates commonlyexhibit phenotypic matching of digestive enzyme and/or transportactivity to changes in major caloric substrates, as predicted by theADH. The regulation of these activities may involve interactionsamong various cell types and includes responses on time scalesranging from minutes to days. New evidence outlines molecular andcellular interactions regulating apparently synchronous changes inthe transcription of enzymes and transporters in response to higherlevels of dietary carbohydrate; however, further research is necessaryto determine whether such changes reflect actual or pseudocoordination.Overall, the study of molecular regulatory mechanismsin both hosts and their microbiomes across animal taxa will shed lighton the coordination of digestive adaptation and modulation.