Differential Engagement of Fermentative Taxa in Gut Contents of the Earthworm Lumbricus terrestris

Abstract

ABSTRACT The earthworm gut is an anoxic, saccharide-rich microzone in aerated 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 gut contents of L. terrestris . This hypothesis was addressed by (i) assessing the fermentation profiles of anoxic gut content microcosms that were supplemented with gut-associated saccharides and (ii) the concomitant phylogenic analysis of 16S rRNA sequences. Galactose, glucose, maltose, mannose, arabinose, fucose, rhamnose, and xylose stimulated the production of fermentation products, including H 2 , CO 2 , acetate, lactate, propionate, formate, succinate, and ethanol. Fermentation profiles were dependent on the supplemental saccharide (e.g., glucose yielded large amounts of H 2 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 saccharide stimulated a subset of the diverse phylotypes. An Aeromonas -related phylotype displayed a high relative abundance in all treatments, whereas key Enterobacteriaceae -affiliated phylotypes were stimulated by some but not all saccharides. Collectively, these results reinforce the likelihood that (i) different saccharides stimulate different fermentations in gut contents of the earthworm and (ii) facultative aerobes related to Aeromonadaceae and Enterobacteriaceae can be important drivers of these fermentations. IMPORTANCE The feeding habits of earthworms influence the turnover of elements in the terrestrial biosphere. The alimentary tract of the earthworm constitutes an anoxic saccharide-rich microzone in aerated soils that offers ingested microbes a unique opportunity for anaerobic growth. The fermentative activity of microbes in the alimentary tract are responsible for the in situ production of (i) organic compounds that can be assimilated by the earthworm and (ii) H 2 that is subject to in vivo emission by the earthworm and can be trophically linked to secondary microbial events in soils. To gain insight on how fermentative members of the gut microbiome might respond to the saccharide-rich alimentary canal, this study examines the impact of diverse gut-associated saccharides on the differential activation of fermentative microbes in gut contents of the model earthworm L. terrestris .