Viehboeck, T.; Krause, N.; Weber, P. M.; O'Shea, E.; Noetzel, V.; Pende, N.; Goelles-Kirth, H.; Varoquaux, N.; Boccard, F.; Junier, I.; Lioy, V. S.; Bulgheresi, S.

Bacterial chromosome biology has largely focused on bacteria that are either free-living or facultatively associated with eukaryotes. Therefore, it is not known how obligate animal symbionts organize their chromosomes. Here, we studied the chromosome organization of three species of multicellular Neisseriaceae that colonize the oral cavity of mammals, Alysiella filiformis, Simonsiella muelleri and Conchiformibius steedae. DNA fluorescence in situ hybridization showed that, irrespective of their ploidy, their chromosomes are longitudinally configured with the origin of DNA replication consistently localized at their host-attached poles throughout the cell cycle. Immunolocalization, ChIP-seq and EMSA implicated ParBS complexes in maintaining this stable chromosome orientation. Moreover, chromosome conformation capture across two species and three growth conditions further revealed conserved lifestyle-associated chromosome architectures, including planktonic-specific ParB-associated chromatin loops and condition-specific chromatin frontiers. Together, our findings show that obligate mammalian symbionts maintain stable longitudinal chromosome orientations irrespective of ploidy while remodeling higher-order chromosome architecture according to physiological state. Distinct yet conserved chromosome architectures characterize exponential, stationary and surface-associated growth, indicating that bacterial genome folding reflects lifestyle and environmental context.