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Dual function of OmpM as outer membrane tether and nutrient uptake channel in diderm Firmicutes

Dual function of OmpM as outer membrane tether and nutrient uptake channel in diderm Firmicutes
Dual function of OmpM as outer membrane tether and nutrient uptake channel in diderm Firmicutes

The outer membrane (OM) in diderm, or Gram-negative, bacteria must be tethered to peptidoglycan for mechanical stability and to maintain cell morphology. Most diderm phyla from the Terrabacteria group have recently been shown to lack well-characterised OM attachment systems, but instead have OmpM, which could represent an ancestral tethering system in bacteria. Here, we have determined the structure of the most abundant OmpM protein from Veillonella parvula (diderm Firmicutes) by single particle cryogenic electron microscopy. We also characterised the channel properties of the transmembrane β-barrel of OmpM and investigated the structure and PG-binding properties of its periplasmic stalk region. Our results show that OM tethering and nutrient acquisition are genetically linked in V. parvula, and probably other diderm Terrabacteria. This dual function of OmpM may have played a role in the loss of the OM in ancestral bacteria and the emergence of monoderm bacterial lineages.

Firmicutes, Cell Membrane/metabolism, Cell Wall/metabolism, Bacteria/metabolism, Gram-Negative Bacteria/metabolism, Nutrients, Bacterial Outer Membrane Proteins/metabolism
2041-1723
7152
Silale, Augustinas
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Zhu, Yiling
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Witwinowski, Jerzy
2017a728-d4f8-4a56-a3e7-0ddf41f29c2d
Smith, Robert E.
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Newman, Kahlan E.
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Bhamidimarri, Satya P.
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Baslé, Arnaud
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Khalid, Syma
90fbd954-7248-4f47-9525-4d6af9636394
Beloin, Christophe
5d163b35-ad48-425e-aac2-093875f825b7
Gribaldo, Simonetta
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van den Berg, Bert
d24aad29-10a4-4ffa-b893-58ba00a413f0
Silale, Augustinas
5df78a5e-dc0a-48a2-b150-860e4f71ab12
Zhu, Yiling
a9e10808-eb8b-47f2-b1ac-906eca2e8555
Witwinowski, Jerzy
2017a728-d4f8-4a56-a3e7-0ddf41f29c2d
Smith, Robert E.
8f61ac54-7472-4be3-a15c-076bbdaf9749
Newman, Kahlan E.
7fccd66d-2aa1-4dd6-b477-2ad528389f83
Bhamidimarri, Satya P.
743238c8-95bc-4b19-93c5-76117dc36b44
Baslé, Arnaud
73397e8c-9ea9-4426-bd78-8df9205a8803
Khalid, Syma
90fbd954-7248-4f47-9525-4d6af9636394
Beloin, Christophe
5d163b35-ad48-425e-aac2-093875f825b7
Gribaldo, Simonetta
70c3d33e-d8b2-4ec6-9c3a-d7388aa570fa
van den Berg, Bert
d24aad29-10a4-4ffa-b893-58ba00a413f0

Silale, Augustinas, Zhu, Yiling, Witwinowski, Jerzy, Smith, Robert E., Newman, Kahlan E., Bhamidimarri, Satya P., Baslé, Arnaud, Khalid, Syma, Beloin, Christophe, Gribaldo, Simonetta and van den Berg, Bert (2023) Dual function of OmpM as outer membrane tether and nutrient uptake channel in diderm Firmicutes. Nature Communications, 14 (1), 7152, [7152]. (doi:10.1038/s41467-023-42601-y).

Record type: Article

Abstract

The outer membrane (OM) in diderm, or Gram-negative, bacteria must be tethered to peptidoglycan for mechanical stability and to maintain cell morphology. Most diderm phyla from the Terrabacteria group have recently been shown to lack well-characterised OM attachment systems, but instead have OmpM, which could represent an ancestral tethering system in bacteria. Here, we have determined the structure of the most abundant OmpM protein from Veillonella parvula (diderm Firmicutes) by single particle cryogenic electron microscopy. We also characterised the channel properties of the transmembrane β-barrel of OmpM and investigated the structure and PG-binding properties of its periplasmic stalk region. Our results show that OM tethering and nutrient acquisition are genetically linked in V. parvula, and probably other diderm Terrabacteria. This dual function of OmpM may have played a role in the loss of the OM in ancestral bacteria and the emergence of monoderm bacterial lineages.

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Accepted/In Press date: 16 October 2023
e-pub ahead of print date: 6 November 2023
Published date: 6 November 2023
Additional Information: Funding Information: We thank the University of York (UK) electron cryo-microscopy facility for access to instrumentation and support. We acknowledge the Diamond Light Source for I03 beamline access (proposal mx-24948) and support. We thank David Staunton (University of Oxford) for carrying out the dynamic scanning calorimetry experiments. This work was supported by a Wellcome Trust Investigator award (214222/Z/18/Z) to B.v.d.B., providing salary support to A.S. and Y.Z. C.B., S.G., J.W., and R.E.S. were supported by funding from the French National Research Agency (ANR) (no. Fir-OM ANR-16-CE12-0010), the Institut Pasteur Programmes Transversaux de Recherche (no. PTR 39-16), and the French government Investissement d’Avenir Program, Laboratoire d’Excellence Integrative Biology of Emerging Infectious Diseases (grant no. ANR-10-LABX-62-IBEID). The authors acknowledge the use of the IRIDIS High Performance Computing Facility, and associated support services at the University of Southampton, in the completion of this work. K.E.N. was supported by a Ph.D. Studentship from the Engineering and Physical Sciences Research Council (Project Number: 2446840), and S.K. by an EPSRC established Career Fellowship (EPSRC grant no. EP/V030779/1). Funding Information: We thank the University of York (UK) electron cryo-microscopy facility for access to instrumentation and support. We acknowledge the Diamond Light Source for I03 beamline access (proposal mx-24948) and support. We thank David Staunton (University of Oxford) for carrying out the dynamic scanning calorimetry experiments. This work was supported by a Wellcome Trust Investigator award (214222/Z/18/Z) to B.v.d.B., providing salary support to A.S. and Y.Z. C.B., S.G., J.W., and R.E.S. were supported by funding from the French National Research Agency (ANR) (no. Fir-OM ANR-16-CE12-0010), the Institut Pasteur Programmes Transversaux de Recherche (no. PTR 39-16), and the French government Investissement d’Avenir Program, Laboratoire d’Excellence Integrative Biology of Emerging Infectious Diseases (grant no. ANR-10-LABX-62-IBEID). The authors acknowledge the use of the IRIDIS High Performance Computing Facility, and associated support services at the University of Southampton, in the completion of this work. K.E.N. was supported by a Ph.D. Studentship from the Engineering and Physical Sciences Research Council (Project Number: 2446840), and S.K. by an EPSRC established Career Fellowship (EPSRC grant no. EP/V030779/1). © 2023. The Author(s).
Keywords: Firmicutes, Cell Membrane/metabolism, Cell Wall/metabolism, Bacteria/metabolism, Gram-Negative Bacteria/metabolism, Nutrients, Bacterial Outer Membrane Proteins/metabolism

Identifiers

Local EPrints ID: 484810
URI: http://eprints.soton.ac.uk/id/eprint/484810
ISSN: 2041-1723
PURE UUID: 9706eaeb-3494-426c-bc6c-2d154aa224c6
ORCID for Syma Khalid: ORCID iD orcid.org/0000-0002-3694-5044

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Date deposited: 22 Nov 2023 17:32
Last modified: 06 Jun 2024 01:45

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Contributors

Author: Augustinas Silale
Author: Yiling Zhu
Author: Jerzy Witwinowski
Author: Robert E. Smith
Author: Kahlan E. Newman
Author: Satya P. Bhamidimarri
Author: Arnaud Baslé
Author: Syma Khalid ORCID iD
Author: Christophe Beloin
Author: Simonetta Gribaldo
Author: Bert van den Berg

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