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The hitchhiker's guide to the periplasm: unexpected molecular interactions of polymyxin B1 in E. coli

The hitchhiker's guide to the periplasm: unexpected molecular interactions of polymyxin B1 in E. coli
The hitchhiker's guide to the periplasm: unexpected molecular interactions of polymyxin B1 in E. coli
The periplasm of Gram-negative bacteria is a complex, highly crowded molecular environment. Little is known about how antibiotics move across the periplasm and the interactions they experience. Here, atomistic molecular dynamics simulations are used to study the antibiotic polymyxin B1 within models of the periplasm, which are crowded to different extents. We show that PMB1 is likely to be able to “hitchhike” within the periplasm by binding to lipoprotein carriers—a previously unreported passive transport route. The simulations reveal that PMB1 forms both transient and long-lived interactions with proteins, osmolytes, lipids of the outer membrane, and the cell wall, and is rarely uncomplexed when in the periplasm. Furthermore, it can interfere in the conformational dynamics of native proteins. These are important considerations for interpreting its mechanism of action and are likely to also hold for other antibiotics that rely on diffusion to cross the periplasm.
Braun's lipoprotein, OmpA, Pal, antibiotics, cell envelope, cell wall, crowded environment, crowded periplasm, lipoproteins, molecular dynamics, polymyxin B1
0969-2126
444-456.e2
Pedebos, Conrado
87801080-118f-4814-8f86-3524184b0d88
Smith, Iain Peter Shand
16d4b544-dc39-49db-9d14-15b5eb4d295d
Boags, Alister
ec8b83d9-0601-4c97-8acc-3a26349a3076
Khalid, Syma
90fbd954-7248-4f47-9525-4d6af9636394
Pedebos, Conrado
87801080-118f-4814-8f86-3524184b0d88
Smith, Iain Peter Shand
16d4b544-dc39-49db-9d14-15b5eb4d295d
Boags, Alister
ec8b83d9-0601-4c97-8acc-3a26349a3076
Khalid, Syma
90fbd954-7248-4f47-9525-4d6af9636394

Pedebos, Conrado, Smith, Iain Peter Shand, Boags, Alister and Khalid, Syma (2021) The hitchhiker's guide to the periplasm: unexpected molecular interactions of polymyxin B1 in E. coli. Structure, 29 (5), 444-456.e2. (doi:10.1016/j.str.2021.01.009).

Record type: Article

Abstract

The periplasm of Gram-negative bacteria is a complex, highly crowded molecular environment. Little is known about how antibiotics move across the periplasm and the interactions they experience. Here, atomistic molecular dynamics simulations are used to study the antibiotic polymyxin B1 within models of the periplasm, which are crowded to different extents. We show that PMB1 is likely to be able to “hitchhike” within the periplasm by binding to lipoprotein carriers—a previously unreported passive transport route. The simulations reveal that PMB1 forms both transient and long-lived interactions with proteins, osmolytes, lipids of the outer membrane, and the cell wall, and is rarely uncomplexed when in the periplasm. Furthermore, it can interfere in the conformational dynamics of native proteins. These are important considerations for interpreting its mechanism of action and are likely to also hold for other antibiotics that rely on diffusion to cross the periplasm.

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Structure_manuscript_PMB1_with_SI - Accepted Manuscript
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More information

Accepted/In Press date: 21 January 2021
e-pub ahead of print date: 11 February 2021
Published date: 6 May 2021
Keywords: Braun's lipoprotein, OmpA, Pal, antibiotics, cell envelope, cell wall, crowded environment, crowded periplasm, lipoproteins, molecular dynamics, polymyxin B1

Identifiers

Local EPrints ID: 448784
URI: http://eprints.soton.ac.uk/id/eprint/448784
ISSN: 0969-2126
PURE UUID: 3a6df657-8a97-4fb3-8b76-e71f99c3fb17
ORCID for Alister Boags: ORCID iD orcid.org/0000-0003-3072-3720
ORCID for Syma Khalid: ORCID iD orcid.org/0000-0002-3694-5044

Catalogue record

Date deposited: 05 May 2021 16:55
Last modified: 17 Mar 2024 06:31

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Contributors

Author: Conrado Pedebos
Author: Iain Peter Shand Smith
Author: Alister Boags ORCID iD
Author: Syma Khalid ORCID iD

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