Mucispirillum schaedleri is an abundant inhabitant of the intestinal mucus layer of rodents and other animals. We analyzed the genome and transcriptome of M. schaedleri ASF 457 to gain insights into its lifestyle and tested traits predicted by the genome with physiological experiments. Surprisingly, though thought to be a mucus degrader its genome predicts that M. schaedleri has limited capacity for degrading host-derived mucosal glycans or other complex polysaccharides. It may rather 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 survival close to the mucosal tissue blooms during inflammation. Interestingly, M. schaedleri harbors a type VI secretion system (T6SS) and several putative effector proteins containing eukaryotic domains, which may be involved in interacting with the host and may play a role in inflammation. An examination of individual phylogenies of all genes in the M. schaedleri genome indicated extensive lateral gene transfer, primarily from intestinal Epsilon- and Deltaproteobacteria. Though M. schaedleri utilizes non-laterally-transferred pathways (e.g. nitrate reduction), laterally acquired pathways from gut organisms (e.g. T6SS and glycerol-P utilization) are 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.