Biogenesis of a Bacterial Organelle: The Carboxysome Assembly Pathway

•A system to control and visualize de novo carboxysome biogenesis was developed•Carboxysome biogenesis starts as RuBisCO aggregates into a procarboxysome via CcmM•Shell encapsulation of the procarboxysome requires CcmN, CcmK2, and CcmO•The core of carboxysomes forms first, before being surrounded by a protein shell

SummaryThe carboxysome is a protein-based organelle for carbon fixation in cyanobacteria, keystone organisms in the global carbon cycle. It is composed of thousands of subunits including hexameric and pentameric proteins that form a shell to encapsulate the enzymes ribulose 1,5-bisphosphate carboxylase/oxygenase and carbonic anhydrase. Here, we describe the stages of carboxysome assembly and the requisite gene products necessary for progression through each. Our results demonstrate that, unlike membrane-bound organelles of eukaryotes, in carboxysomes the interior of the compartment forms first, at a distinct site within the cell. Subsequently, shell proteins encapsulate this procarboxysome, inducing budding and distribution of functional organelles within the cell. We propose that the principles of carboxysome assembly that we have uncovered extend to diverse bacterial microcompartments.

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