Fermentation in Earthworm Gut Content

The earthworm gut is an anoxic, saccharide-rich microzone in oxic soils. The apparent degradation of diverse saccharides in the alimentary canal of the model earthworm Lumbricus terrestris is concomitant with the production of diverse organic acids, indicating that fermentation is an ongoing process in the earthworm gut. However, little is known about how different gut-associated saccharides are fermented. The hypothesis of this investigation was that different gut-associated saccharides differentially stimulate fermentative microorganisms in the gut of L. terrestris. This hypothesis was addressed by (a) assessing the fermentation profiles of anoxic gut content microcosms (i.e., anoxic slurries) that were supplemented with gut-associated saccharides and (b) the concomitant phylogenic analysis of 16S rRNA sequences. Galactose, glucose, maltose, mannose, arabinose, fucose, rhamnose, and xylose stimulated the production of fermentation products, including H2, CO2, acetate, lactate, propionate, formate, succinate, and ethanol. Fermentation product profiles were dependent on the supplemental saccharide (e.g., glucose yielded large amounts of H2 and ethanol whereas fucose did not, and maltose yielded large amounts of lactate whereas mannose did not). Approximately 1,750,000 16S rRNA sequences were affiliated with 37 families, and phylogenic analyses indicated that a respective sugar stimulated a subset of the gut microbiome. Of the diverse species-level phylotypes detected, Aeromonas-affiliated phylotype A was the most abundant phylotype in all saccharide-supplemented microcosms, whereas Enterobacteriaceae-affiliated phylotypes E,C and R were stimulated by some but not all saccharides. Collectively, these results reinforce the likelihood that (a) different saccharides stimulate different fermentations in the earthworm alimentary canal, and (b) facultative aerobes related to Enterobacteriaceae and Aeromonadaceae are important drivers of these fermentations during gut passage.