Mucispirillum schaedleri is an abundant inhabitant of the intestinal mucus layer of rodents and other animals. To gain insights into its lifestyle, we analyzed the genome and transcriptome of M. schaedleri ASF 457 and tested for traits predicted by the genome using physiological experiments. Although thought to be a mucus degrader, its genome surprisingly predicts that M. schaedleri has limited capacity for degrading host-derived mucosal glycans or other complex polysaccharides. Rather, it may utilize small compounds such as peptides, amino acids, glycerol, and short chain fatty acids. Additionally, it can reduce nitrate and has systems for scavenging oxygen and reactive oxygen species, which accounts for its presence close to the mucosal tissue and during inflammation. Also of note, M. schaedleri harbors a type VI secretion system (T6SS) and several putative effector proteins containing eukaryotic domains, which suggest intimate interactions with the host and a role in inflammation. Examination of the individual phylogenies of all genes in the M. schaedleri genome revealed extensive horizontal gene transfer, primarily from intestinal Epsilon- and Deltaproteobacteria. Though M. schaedleri utilizes non-horizontally-transferred pathways (e.g. nitrate reduction), horizontally-acquired pathways from gut organisms (e.g. T6SS and glycerol-P utilization) are also likely also important for its survival in the intestine, suggesting that lateral gene transfer may have played a key role in facilitating its establishment in the gut ecosystem.