Journal
JOURNAL OF MOLECULAR BIOLOGY
Volume 430, Issue 21, Pages 4156-4167Publisher
ACADEMIC PRESS LTD- ELSEVIER SCIENCE LTD
DOI: 10.1016/j.jmb.2018.08.013
Keywords
RuBisCO; carboxysome biogenesis; zernike phase-contrast cryo-electron tomography; convolutional neural network-based annotation; molecular dynamics simulation
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Funding
- National Institutes of Health [P41GM103832, R01GM037657, R01GM080139]
- Robert Welch Foundation [Q1242, H-0037]
- NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES [P41GM103832, R01GM037657, R01GM080139] Funding Source: NIH RePORTER
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Cyanobacteria are photosynthetic organisms responsible for similar to 25% of the organic carbon fixation on earth. A key step in carbon fixation is catalyzed by ribulose bisphosphate carboxylase/oxygenase (RuBisCO), the most abundant enzyme in the biosphere. Applying Zernike phase-contrast electron cryo-tomography and automated annotation, we identified individual RuBisCO molecules and their assembly intermediates leading to the formation of carboxysomes inside Syn5 cyanophage infected cyanobacteria Synechococcus sp. WH8109 cells. Surprisingly, more RuBisCO molecules were found to be present as cytosolic free-standing complexes or clusters than as packaged assemblies inside carboxysomes. Cytosolic RuBisCO clusters and partially assembled carboxysomes identified in the cell tomograms support a concurrent assembly model involving both the protein shell and the enclosed RuBisCO. In mature carboxysomes, RuBisCO is neither randomly nor strictly icosahedrally packed within protein shells of variable sizes. A time-averaged molecular dynamics simulation showed a semi-liquid probability distribution of the RuBisCO in carboxysomes and correlated well with carboxysome subtomogram averages. Our structural observations reveal the various stages of RuBisCO assemblies, which could be important for understanding cellular function. (C) 2018 Elsevier Ltd. All rights reserved.
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