Assembly, function and evolution of cyanobacterial carboxysomes

Area of Science:

• Microbiology
• Biochemistry
• Evolutionary Biology

Background:

• Cyanobacteria utilize carboxysomes, specialized bacterial microcompartments, to encapsulate the enzyme RuBisCO.
• Two primary types of carboxysomes, alpha and beta, exhibit significant differences in their composition, assembly mechanisms, and evolutionary origins.

Purpose of the Study:

• To elucidate the distinct evolutionary trajectories and assembly processes of alpha and beta carboxysomes.
• To explore the potential of carboxysomes as modules for synthetic biology applications.

Main Methods:

• Comparative analysis of gene organization and protein components.
• Phylogenetic analysis of conserved shell proteins.
• Investigation of assembly pathways, including the role of encapsulation peptides.
• Exploration of heterologous expression and redesign for synthetic biology.

Main Results:

• Alpha carboxysomes show conserved gene organization, suggesting horizontal gene transfer, and co-assemble with cargo enzymes.
• Beta carboxysomes assemble an enzymatic core first, relying on an encapsulation peptide for shell formation.
• Phylogenetic and assembly data suggest beta carboxysomes are more closely related to bacterial metabolosomes than alpha carboxysomes.
• Beta carboxysomes, found in basal cyanobacterial clades, can encapsulate ancestrally reconstructed RuBisCO, indicating an ancient origin.

Conclusions:

• Alpha and beta carboxysomes represent distinct evolutionary lineages with unique assembly strategies.
• The ancient origin of beta carboxysomes is supported by their presence in basal cyanobacteria and ability to encapsulate reconstructed RuBisCO.
• Both carboxysome types are promising genetic/metabolic modules for synthetic biology, with recent advances in heterologous expression and redesign.