Three-Dimensional Structure of the Ultraoligotrophic Marine Bacterium “Candidatus Pelagibacter ubique”

SAR11 bacteria are small, heterotrophic, marine α-proteobacteria found throughout the oceans. They thrive at the low nutrient concentrations typical of open ocean conditions, although the adaptations required for life under these conditions are not well understood. To illuminate this issue we used cryo-electron tomography to study Pelagibacter , strain HTCC1062, a member of SAR11 clade. Our results revealed its cellular dimensions and details of its intracellular organization. The frozen-hydrated cells, which are preserved in a life-like state, have an average cell volume (enclosed by outer membrane) of 0.037 ± 0.011 μm 3 . Strikingly, the periplasmic space occupies ∼20% - 50% of the total cell volume in log phase cells and ∼50% - 70% in stationary phase cells. Within the cell, the nucleoid occupies the convex side of the crescent-shaped cell, and the ribosomes occupy predominantly the remaining concave side at a relatively high concentration of 10,000 – 12,000 per μm 3 . An outer membrane pore complex that is likely composed of PilQ, was frequently observed in both log and stationary phases. Long filaments, most likely type-IV pili, were found on dividing cells. The physical dimensions, intracellular organization, and morphological changes throughout the life cycle of Pelagibacter provide structural insights into the functional adaptions of these oligotrophic ultramicrobacteria to their habitat. IMPORTANCE Bacterioplankton, SAR11 clade (Pelagibacterales), are of interest because of their global, biogeochemical significance, and because they appear to have been molded by unusual evolutionary circumstances that favor simplicity and efficiency. They have adapted to an ecosystem where nutrient concentrations hover near the extreme limits at which transport systems can function adequately and evolved streamlined genomes to execute only functions essential for life. However, little is known about the accurate size limitation and cellular features of living oligotrophic ultramicrobacteria. In this study, we have used cryo-electron tomography (cryo-ET) to obtain accurate physical information about the cellular architecture of Pelagibacter, the first cultivated member of SAR11 clade. These results provide foundational information for answering questions about cell architecture and function in these ultra-small oligotrophic bacteria.