The Structural Diversity of Encapsulin Protein Shells

Overview

Journal Chembiochem

Specialty Biochemistry

Date 2024 Sep 27

PMID 39330624

Authors

Tobias W Giessen

Affiliations

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Abstract

Subcellular compartmentalization is a universal feature of all cells. Spatially distinct compartments, be they lipid- or protein-based, enable cells to optimize local reaction environments, store nutrients, and sequester toxic processes. Prokaryotes generally lack intracellular membrane systems and usually rely on protein-based compartments and organelles to regulate and optimize their metabolism. Encapsulins are one of the most diverse and widespread classes of prokaryotic protein compartments. They self-assemble into icosahedral protein shells and are able to specifically internalize dedicated cargo enzymes. This review discusses the structural diversity of encapsulin protein shells, focusing on shell assembly, symmetry, and dynamics. The properties and functions of pores found within encapsulin shells will also be discussed. In addition, fusion and insertion domains embedded within encapsulin shell protomers will be highlighted. Finally, future research directions for basic encapsulin biology, with a focus on the structural understand of encapsulins, are briefly outlined.

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References

Jones J, Benisch R, Giessen T . Encapsulin cargo loading: progress and potential. J Mater Chem B. 2023; 11(20):4377-4388. PMC: 10225969. DOI: 10.1039/d3tb00288h. View

Wikoff W, Liljas L, Duda R, Tsuruta H, Hendrix R, Johnson J . Topologically linked protein rings in the bacteriophage HK97 capsid. Science. 2000; 289(5487):2129-33. DOI: 10.1126/science.289.5487.2129. View

Altenburg W, Rollins N, Silver P, Giessen T . Exploring targeting peptide-shell interactions in encapsulin nanocompartments. Sci Rep. 2021; 11(1):4951. PMC: 7925596. DOI: 10.1038/s41598-021-84329-z. View

Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar G, Sonnhammer E . Pfam: The protein families database in 2021. Nucleic Acids Res. 2020; 49(D1):D412-D419. PMC: 7779014. DOI: 10.1093/nar/gkaa913. View

Johnson J, Speir J . Quasi-equivalent viruses: a paradigm for protein assemblies. J Mol Biol. 1997; 269(5):665-75. DOI: 10.1006/jmbi.1997.1068. View

Kerfeld C, Heinhorst S, Cannon G . Bacterial microcompartments. Annu Rev Microbiol. 2010; 64:391-408. DOI: 10.1146/annurev.micro.112408.134211. View

LaFrance B, Cassidy-Amstutz C, Nichols R, Oltrogge L, Nogales E, Savage D . The encapsulin from Thermotoga maritima is a flavoprotein with a symmetry matched ferritin-like cargo protein. Sci Rep. 2021; 11(1):22810. PMC: 8610991. DOI: 10.1038/s41598-021-01932-w. View

He D, Hughes S, Vanden-Hehir S, Georgiev A, Altenbach K, Tarrant E . Structural characterization of encapsulated ferritin provides insight into iron storage in bacterial nanocompartments. Elife. 2016; 5. PMC: 5012862. DOI: 10.7554/eLife.18972. View

Adamson L, Tasneem N, Andreas M, Close W, Jenner E, Szyszka T . Pore structure controls stability and molecular flux in engineered protein cages. Sci Adv. 2022; 8(5):eabl7346. PMC: 8816334. DOI: 10.1126/sciadv.abl7346. View

10.

Kwon S, Andreas M, Giessen T . Structure and heterogeneity of a highly cargo-loaded encapsulin shell. J Struct Biol. 2023; 215(4):108022. DOI: 10.1016/j.jsb.2023.108022. View

11.

McHugh C, Fontana J, Nemecek D, Cheng N, Aksyuk A, Heymann J . A virus capsid-like nanocompartment that stores iron and protects bacteria from oxidative stress. EMBO J. 2014; 33(17):1896-911. PMC: 4195785. DOI: 10.15252/embj.201488566. View

12.

Ferlez B, Sutter M, Kerfeld C . Glycyl Radical Enzyme-Associated Microcompartments: Redox-Replete Bacterial Organelles. mBio. 2019; 10(1). PMC: 6325248. DOI: 10.1128/mBio.02327-18. View

13.

Kartal B, Keltjens J . Anammox Biochemistry: a Tale of Heme c Proteins. Trends Biochem Sci. 2016; 41(12):998-1011. DOI: 10.1016/j.tibs.2016.08.015. View

14.

Tracey J, Coronado M, Giessen T, Lau M, Silver P, Ward B . The Discovery of Twenty-Eight New Encapsulin Sequences, Including Three in Anammox Bacteria. Sci Rep. 2019; 9(1):20122. PMC: 6934571. DOI: 10.1038/s41598-019-56533-5. View

15.

Andreas M, Giessen T . Large-scale computational discovery and analysis of virus-derived microbial nanocompartments. Nat Commun. 2021; 12(1):4748. PMC: 8346489. DOI: 10.1038/s41467-021-25071-y. View

16.

Jones J, Andreas M, Giessen T . Exploring the Extreme Acid Tolerance of a Dynamic Protein Nanocage. Biomacromolecules. 2023; 24(3):1388-1399. PMC: 10311355. DOI: 10.1021/acs.biomac.2c01424. View

17.

Greening C, Lithgow T . Formation and function of bacterial organelles. Nat Rev Microbiol. 2020; 18(12):677-689. DOI: 10.1038/s41579-020-0413-0. View

18.

Baker M, Jiang W, Rixon F, Chiu W . Common ancestry of herpesviruses and tailed DNA bacteriophages. J Virol. 2005; 79(23):14967-70. PMC: 1287596. DOI: 10.1128/JVI.79.23.14967-14970.2005. View

19.

Parent K, Khayat R, Tu L, Suhanovsky M, Cortines J, Teschke C . P22 coat protein structures reveal a novel mechanism for capsid maturation: stability without auxiliary proteins or chemical crosslinks. Structure. 2010; 18(3):390-401. PMC: 2951021. DOI: 10.1016/j.str.2009.12.014. View

20.

Aussignargues C, Pandelia M, Sutter M, Plegaria J, Zarzycki J, Turmo A . Structure and Function of a Bacterial Microcompartment Shell Protein Engineered to Bind a [4Fe-4S] Cluster. J Am Chem Soc. 2015; 138(16):5262-70. DOI: 10.1021/jacs.5b11734. View