Lifestyle and Horizontal Gene Transfer-Mediated Evolution of Mucispirillum schaedleri, a Core Member of the Murine Gut Microbiota

Abstract

<i>Mucispirillum schaedleri</i> is an abundant inhabitant of the intestinal mucus layer of rodents and other animals and has been suggested to be a pathobiont, a commensal that plays a role in disease. In order to gain insights into its lifestyle, we analyzed the genome and transcriptome of <i>M. schaedleri</i> ASF 457 and performed physiological experiments to test traits predicted by its genome. Although described as a mucus inhabitant, <i>M. schaedleri</i> has limited capacity for degrading host-derived mucosal glycans and other complex polysaccharides. Additionally, <i>M. schaedleri</i> reduces nitrate and expresses systems for scavenging oxygen and reactive oxygen species <i>in vivo</i>, which may account for its localization close to the mucosal tissue and expansion during inflammation. Also of note, <i>M. schaedleri</i> harbors a type VI secretion system and putative effector proteins and can modify gene expression in mucosal tissue, suggesting intimate interactions with its host and a possible role in inflammation. The <i>M. schaedleri</i> genome has been shaped by extensive horizontal gene transfer, primarily from intestinal <i>Epsilon</i>- and <i>Deltaproteobacteria</i>, indicating that horizontal gene transfer has played a key role in defining its niche in the gut ecosystem. <b>IMPORTANCE</b> Shifts in gut microbiota composition have been associated with intestinal inflammation, but it remains unclear whether inflammation-associated bacteria are commensal or detrimental to their host. Here, we studied the lifestyle of the gut bacterium <i>Mucispirillum schaedleri</i>, which is associated with inflammation in widely used mouse models. We found that <i>M. schaedleri</i> has specialized systems to handle oxidative stress during inflammation. Additionally, it expresses secretion systems and effector proteins and can modify the mucosal gene expression of its host. This suggests that <i>M. schaedleri</i> undergoes intimate interactions with its host and may play a role in inflammation. The insights presented here aid our understanding of how commensal gut bacteria may be involved in altering susceptibility to disease.