TY - JOUR
T1 - Three-dimensional structure of the ultraoligotrophic marine bacterium "Candidatus pelagibacter ubique"
AU - Zhao, Xiaowei
AU - Schwartz, Cindi L.
AU - Pierson, Jason
AU - Giovannoni, Stephen J.
AU - McIntosh, J. Richard
AU - Nicastro, Daniela
N1 - Funding Information:
We are grateful to H. J. Tripp and J. C. Cho for providing the Pelagibacter cultures, to Pu Shing Ho for calculating the B-DNA volume, and to Y. W. Chang, Davi Ortega, and G. Jensen for generously providing the PilQ map of M. xanthus and discussing PilQ. We also thank Xiangan Liu for the rotational correlation analysis of the Pelagibacter PilQ density. This work was supported by an NIH grant to J.R.M. (grant RR00592) and a Marine Microbiology Initiative Investigator Grant from the Gordon and Betty Moore Foundation (grant GBMF607.01). The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Publisher Copyright:
© 2017 American Society for Microbiology. All Rights Reserved.
PY - 2017
Y1 - 2017
N2 - 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 ± 0.011 μm3. Strikingly, the periplasmic space occupied ~20% to 50% of the total cell volume in log-phase cells and ~50% 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/μm3. 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.
AB - 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 ± 0.011 μm3. Strikingly, the periplasmic space occupied ~20% to 50% of the total cell volume in log-phase cells and ~50% 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/μm3. 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.
KW - Cryo-electron tomography
KW - PilQ
KW - SAR11
KW - Type IV pili
KW - Ultramicrobacteria
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U2 - 10.1128/AEM.02807-16
DO - 10.1128/AEM.02807-16
M3 - Article
C2 - 27836840
AN - SCOPUS:85010223128
VL - 83
JO - Applied and Environmental Microbiology
JF - Applied and Environmental Microbiology
SN - 0099-2240
IS - 3
M1 - e02807-16
ER -