Metagenomic sequencing provides insights into the location of microbial detoxification in the gut of a small mammalian herbivore

Abstract

Microbial detoxification of plant defense compounds influences the use of certain plants as food sources by herbivores. The location of microbial detoxification along the gut could have profound influences on the distribution, metabolism, and tolerance to toxic compounds. Stephens woodrats (Neotoma stephensi) specialize on juniper, which is heavily defended by numerous defensive compounds, such as oxalate, phenolics, and monoterpenes. Woodrats maintain two gut chambers harboring dense microbial communities: a foregut chamber proximal to the major site of toxin absorption, and a cecal chamber in their hindgut. We performed several experiments to investigate the location of microbial detoxification in the woodrat gut. First, we measured levels of toxins across gut chambers. Compared to food material, oxalate concentrations were immediately lower in the foregut chamber, while concentrations of terpenes remain high in the foregut, and are lowest in the cecal chamber. We also conducted metagenomic sequencing of the foregut and cecal chambers to compare microbial functions. We found that the majority of genes associated with detoxification functions were more abundant in the cecal chamber. However, some genes associated with degradation of oxalate and phenolic compounds were more abundant in the foregut. Thus, it seems that microbial detoxification may take place in various chambers depending on the class of chemical compound. We hypothesize that the location of microbial detoxification could impact the tolerance of animals to these compounds, which may have ecological and evolutionary consequences.