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Molecular principles of the assembly and construction of a carboxysome shell

Lookup NU author(s): Dr Arnaud Basle, Dr Jon Marles-WrightORCiD

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This work is licensed under a Creative Commons Attribution 4.0 International License (CC BY 4.0).


Abstract

© 2024 the Authors, some rights reserved;Intracellular compartmentalization enhances biological reactions, crucial for cellular function and survival. An example is the carboxysome, a bacterial microcompartment for CO2 fixation. The carboxysome uses a polyhedral protein shell made of hexamers, pentamers, and trimers to encapsulate Rubisco, increasing CO2 levels near Rubisco to enhance carboxylation. Despite their role in the global carbon cycle, the molecular mechanisms behind carboxysome shell assembly remain unclear. Here, we present a structural characterization of α-carboxysome shells generated from recombinant systems, which contain all shell proteins and the scaffolding protein CsoS2. Atomic-resolution cryo–electron microscopy of the shell assemblies, with a maximal size of 54 nm, unveil diverse assembly interfaces between shell proteins, detailed interactions of CsoS2 with shell proteins to drive shell assembly, and the formation of heterohexamers and heteropentamers by different shell protein paralogs, facilitating the assembly of larger empty shells. Our findings provide mechanistic insights into the construction principles of α-carboxysome shells and the role of CsoS2 in governing α-carboxysome assembly and functionality.


Publication metadata

Author(s): Wang P, Li J, Li T, Li K, Ng PC, Wang S, Chriscoli V, Basle A, Marles-Wright J, Zhang Y-Z, Liu L-N

Publication type: Article

Publication status: Published

Journal: Science Advances

Year: 2024

Volume: 10

Issue: 48

Online publication date: 29/11/2024

Acceptance date: 25/10/2024

Date deposited: 17/12/2024

ISSN (electronic): 2375-2548

Publisher: American Association for the Advancement of Science

URL: https://doi.org/10.1126/sciadv.adr4227

DOI: 10.1126/sciadv.adr4227

Data Access Statement: The cryo-EM density maps for T = 9, T = 9 Q = 12, T = 13, T = 16, and T = 19 midi-shell as well as CsoS1C-based T = 9 mini-shell have been deposited in the Electron Microscopy Data Bank (EMDB; www.ebi.ac.uk/pdbe/emdb/) with the accession codes EMDB-39598, EMDB-39599, EMD-39601, EMD-39597, EMD-39596, and EMD-50109, respectively. The atomic coordinates for T = 9, T = 9 Q = 12, T = 13, T = 16, and T = 19 midi-shell, as well as CsoS1C-based T = 9 mini-shell and CsoS1A-CsoS1B heteromeric hexamer, have been deposited in the PDB (www.rcsb.org) with the accession codes 8YVE, 8YVF, 8YVI, 8YVD, 8YVC, 9F0H, and 8YXU, respectively. All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials. The midi-shell constructs can be provided by L.-N.L. pending scientific review and a completed material transfer agreement. Requests for the midi-shell constructs should be submitted to L.-N.L.

PubMed id: 39612341


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Funding

Funder referenceFunder name
Biotechnology and Biological Sciences Research Council (BB/V009729/1, BB/Y01135X/1, and BB/Y008308/1)
Leverhulme Trust (RPG-2021-286)
National Key R&D Program of China
National Natural Science Foundation of China
NERC (NE/Z00019X/1)
Royal Society (URF\R\180030)

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