The cryo-EM structure of the S-layer deinoxanthin-binding complex of Deinococcus radiodurans informs properties of its environmental interactions.

DR_2577 S-layer SDBC SlpA amino acid import cell envelope deinoxanthin phosphoglycolipids porins transport properties

Journal

The Journal of biological chemistry
ISSN: 1083-351X
Titre abrégé: J Biol Chem
Pays: United States
ID NLM: 2985121R

Informations de publication

Date de publication:
06 2022
Historique:
received: 13 04 2022
revised: 10 05 2022
accepted: 11 05 2022
pubmed: 17 5 2022
medline: 30 6 2022
entrez: 16 5 2022
Statut: ppublish

Résumé

The radiation-resistant bacterium Deinococcus radiodurans is known as the world's toughest bacterium. The S-layer of D. radiodurans, consisting of several proteins on the surface of the cellular envelope and intimately associated with the outer membrane, has therefore been useful as a model for structural and functional studies. Its main proteinaceous unit, the S-layer deinoxanthin-binding complex (SDBC), is a hetero-oligomeric assembly known to contribute to the resistance against environmental stress and have porin functional features; however, its precise structure is unknown. Here, we resolved the structure of the SDBC at ∼2.5 Å resolution by cryo-EM and assigned the sequence of its main subunit, the protein DR_2577. This structure is characterized by a pore region, a massive β-barrel organization, a stalk region consisting of a trimeric coiled coil, and a collar region at the base of the stalk. We show that each monomer binds three Cu ions and one Fe ion and retains one deinoxanthin molecule and two phosphoglycolipids, all exclusive to D. radiodurans. Finally, electrophysiological characterization of the SDBC shows that it exhibits transport properties with several amino acids. Taken together, these results highlight the SDBC as a robust structure displaying both protection and sieving functions that facilitates exchanges with the environment.

Identifiants

pubmed: 35577074
pii: S0021-9258(22)00471-9
doi: 10.1016/j.jbc.2022.102031
pmc: PMC9189128
pii:
doi:

Substances chimiques

Bacterial Proteins 0
Multiprotein Complexes 0
deinoxanthin 0
Carotenoids 36-88-4

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

102031

Informations de copyright

Copyright © 2022 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Conflict of interest The authors declare that they have no conflicts of interest with the contents of this article.

Références

J Biol Chem. 2020 Mar 27;295(13):4224-4236
pubmed: 32071085
J Mol Biol. 2016 Nov 6;428(22):4528-4543
pubmed: 27693650
Trends Biotechnol. 1997 Jan;15(1):20-6
pubmed: 9032989
J Biol Chem. 1989 Nov 5;264(31):18667-72
pubmed: 2808391
Nature. 2012 Jul 5;487(7405):119-22
pubmed: 22722836
FEMS Microbiol Rev. 1997 Jun;20(1-2):47-98
pubmed: 9276928
FEMS Microbiol Rev. 1997 Jun;20(1-2):25-46
pubmed: 9276927
Structure. 2021 Nov 4;29(11):1279-1285.e3
pubmed: 34265277
Front Microbiol. 2016 Feb 16;7:155
pubmed: 26909071
J Phys Chem B. 2012 Apr 19;116(15):4433-8
pubmed: 22369436
J Bacteriol. 1991 Jan;173(2):457-62
pubmed: 1987140
J Struct Biol. 1999 Dec 1;128(1):82-97
pubmed: 10600563
J Comput Chem. 2004 Oct;25(13):1605-12
pubmed: 15264254
Biochim Biophys Acta. 2014 Jul;1838(7):1978-84
pubmed: 24589688
Photochem Photobiol Sci. 2018 Jan 17;17(1):81-88
pubmed: 29218340
J Mol Biol. 1986 Jan 20;187(2):241-50
pubmed: 3701865
J Struct Biol. 2016 Jan;193(1):1-12
pubmed: 26592709
Nat Methods. 2017 Mar;14(3):290-296
pubmed: 28165473
Front Microbiol. 2015 Jun 03;6:414
pubmed: 26074883
Front Microbiol. 2019 Jun 28;10:1450
pubmed: 31333601
J Bacteriol. 1995 May;177(9):2567-71
pubmed: 7730293
J Struct Biol. 2005 Oct;152(1):36-51
pubmed: 16182563
Nat Microbiol. 2017 Apr 18;2:17059
pubmed: 28418382
Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2126-32
pubmed: 15572765
J Biol Chem. 1985 Oct 5;260(22):12219-23
pubmed: 4044593
Acta Crystallogr D Struct Biol. 2019 Oct 1;75(Pt 10):861-877
pubmed: 31588918
Nat Protoc. 2018 May;13(5):1062-1090
pubmed: 29674755
Commun Biol. 2019 Jun 19;2:218
pubmed: 31240256
Nat Methods. 2017 Apr;14(4):331-332
pubmed: 28250466
J Biol Chem. 1996 Aug 23;271(34):20676-80
pubmed: 8702817
Radiat Res. 1975 Feb;61(2):204-15
pubmed: 803316
J Struct Biol. 1997 Jul;119(2):149-57
pubmed: 9245755
Photochem Photobiol Sci. 2020 Apr 15;19(4):495-503
pubmed: 32236233
Microb Physiol. 2021;31(1):1-15
pubmed: 33341800
Microbiology (Reading). 2006 Sep;152(Pt 9):2779-2787
pubmed: 16946272
J Struct Biol. 2012 Dec;180(3):519-30
pubmed: 23000701

Auteurs

Domenica Farci (D)

Department of Plant Physiology, Warsaw University of Life Sciences - SGGW, Warsaw, Poland; Department of Chemistry, Umeå University, Umeå, Sweden. Electronic address: domenica.farci@umu.se.

Patrycja Haniewicz (P)

Department of Plant Physiology, Warsaw University of Life Sciences - SGGW, Warsaw, Poland.

Daniele de Sanctis (D)

Structural Biology Group, ESRF, The European Synchrotron Radiation Facility, Grenoble, France.

Luca Iesu (L)

Laboratory of Plant Physiology and Photobiology, Department of Life and Environmental Sciences, University of Cagliari, Cagliari, Italy.

Sami Kereïche (S)

Institute of Biology and Medical Genetics, First Faculty of Medicine, Charles University, Prague, Czech Republic.

Mathias Winterhalter (M)

Department of Life Sciences & Chemistry, Jacobs University Bremen, Bremen, Germany.

Dario Piano (D)

Department of Plant Physiology, Warsaw University of Life Sciences - SGGW, Warsaw, Poland; Laboratory of Plant Physiology and Photobiology, Department of Life and Environmental Sciences, University of Cagliari, Cagliari, Italy. Electronic address: dario.piano@unica.it.

Articles similaires

Photosynthesis Ribulose-Bisphosphate Carboxylase Carbon Dioxide Molecular Dynamics Simulation Cyanobacteria

Two codependent routes lead to high-level MRSA.

Abimbola Feyisara Adedeji-Olulana, Katarzyna Wacnik, Lucia Lafage et al.
1.00
Methicillin-Resistant Staphylococcus aureus Penicillin-Binding Proteins Peptidoglycan Bacterial Proteins Anti-Bacterial Agents
Cryoelectron Microscopy Algorithms Image Processing, Computer-Assisted Consensus Software

Classifications MeSH