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

Abstract

SAR11 bacteria are small, heterotrophic, marine alphaproteobacteria found throughout the oceans. They thrive at the low nutrient concentrations typical of open ocean conditions, although the adaptations required for life under those conditions are not well understood. To illuminate this issue, we used cryo-electron tomography to study "Candidatus Pelagibacter ubique" strain HTCC1062, a member of the SAR11 clade. Our results revealed its cellular dimensions and details of its intracellular organization. Frozen-hydrated cells, which were preserved in a life-like state, had an average cell volume (enclosed by the outer membrane) of 0.037 Ϯ 0.011 m 3 . Strikingly, the periplasmic space occupied ϳ20% to 50% of the total cell volume in log-phase cells and ϳ50% to 70% in stationary-phase cells. The nucleoid occupied the convex side of the crescent-shaped cells and the ribosomes predominantly occupied the concave side, at a relatively high concentration of 10,000 to 12,000 ribosomes/m 3 . Outer membrane pore complexes, likely composed of PilQ, were frequently observed in both log-phase and stationary-phase cells. 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 "Ca. Pelagibacter ubique" provide structural insights into the functional adaptions of these oligotrophic ultramicrobacteria to their habitat. IMPORTANCE Bacterioplankton of the 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 in which nutrient concentrations are near the extreme limits at which transport systems can function adequately, and they have evolved streamlined genomes to execute only functions essential for life. However, little is known about the actual size limitations and cellular features of living oligotrophic ultramicrobacteria. In this study, we have used cryo-electron tomography to obtain accurate physical information about the cellular architecture of "Candidatus Pelagibacter ubique," the first cultivated member of the SAR11 clade. These results provide foundational information for answering questions about the cell architecture and functions of these ultrasmall oligotrophic bacteria.

Microdiversification in genome-streamlined ubiquitous freshwater Actinobacteria

“…This corresponds to the in situ cell sizes of freshwater Actinobacteria from Lake Zurich (0.012-0.015 μm 3 , Supplementary Table S3) and other lakes (Posch et al, 2009;Šimek et al, 2014). These microbes are thus among the smallest members of the bacterioplankton, matching the small size of other abundant genome-streamlined bacteria ( Supplementary Table S5; Salcher et al, 2011;Ghai et al, 2013;Zhao et al, 2016). Although isolation campaigns were run throughout the growing season , only one strain ('Ca.…”

Biopearling of Interconnected Outer Membrane Vesicle Chains by a Marine Flavobacterium

“…An electron-dense layer was visible on the inner side of the membrane (Fig. 3C), possibly representing peptidoglycan (40). The outer surface had a fuzzy layer ( Fig.…”

SAR11 bacteria have a high affinity and multifunctional glycine betaine transporter

“…The maximal efficiency of uptake is calculated assuming a spherical cell, regardless of morphology, using the equation 3 D / R 2 , where D is the diffusion coefficient of the substrate and R is the radius of the spherical cell. Taking SAR11 cells to be spherical, the radius is calculated to be 2.06 × 10 −5 cm, based on a cell volume of 0.037 um 3 (Zhao et al ., ). The diffusion coefficient for GBT has been measured to be 9.4 × 10 −7 cm 2 s −1 (Grant and Blackband, ).…”