Systematic comparison of unilamellar vesicles reveals that archaeal core lipid membranes are more permeable than bacterial membranes
dc.contributor.author | Łapińska, U | |
dc.contributor.author | Glover, G | |
dc.contributor.author | Kahveci, Z | |
dc.contributor.author | Irwin, NAT | |
dc.contributor.author | Milner, DS | |
dc.contributor.author | Tourte, M | |
dc.contributor.author | Albers, S-V | |
dc.contributor.author | Santoro, AE | |
dc.contributor.author | Richards, TA | |
dc.contributor.author | Pagliara, S | |
dc.date.accessioned | 2023-05-02T10:39:19Z | |
dc.date.issued | 2023-04 | |
dc.date.updated | 2023-05-02T10:09:34Z | |
dc.description.abstract | One of the deepest branches in the tree of life separates the Archaea from the Bacteria. These prokaryotic groups have distinct cellular systems including fundamentally different phospholipid membrane bilayers. This dichotomy has been termed the lipid divide and possibly bestows different biophysical and biochemical characteristics on each cell type. Classic experiments suggest that bacterial membranes (formed from lipids extracted from Escherichia coli, for example) show permeability to key metabolites comparable to archaeal membranes (formed from lipids extracted from Halobacterium salinarum), yet systematic analyses based on direct measurements of membrane permeability are absent. Here, we develop a new approach for assessing the membrane permeability of approximately 10 μm unilamellar vesicles, consisting of an aqueous medium enclosed by a single lipid bilayer. Comparing the permeability of 18 metabolites demonstrates that diether glycerol-1-phosphate lipids with methyl branches, often the most abundant membrane lipids of sampled archaea, are permeable to a wide range of compounds useful for core metabolic networks, including amino acids, sugars, and nucleobases. Permeability is significantly lower in diester glycerol-3-phosphate lipids without methyl branches, the common building block of bacterial membranes. To identify the membrane characteristics that determine permeability, we use this experimental platform to test a variety of lipid forms bearing a diversity of intermediate characteristics. We found that increased membrane permeability is dependent on both the methyl branches on the lipid tails and the ether bond between the tails and the head group, both of which are present on the archaeal phospholipids. These permeability differences must have had profound effects on the cell physiology and proteome evolution of early prokaryotic forms. To explore this further, we compare the abundance and distribution of transmembrane transporter-encoding protein families present on genomes sampled from across the prokaryotic tree of life. These data demonstrate that archaea tend to have a reduced repertoire of transporter gene families, consistent with increased membrane permeation. These results demonstrate that the lipid divide demarcates a clear difference in permeability function with implications for understanding some of the earliest transitions in cell origins and evolution. | en_GB |
dc.description.sponsorship | Gordon and Betty and Gordon Moore Foundation | en_GB |
dc.description.sponsorship | Biotechnology and Biological Sciences Research Council (BBSRC) | en_GB |
dc.description.sponsorship | European Union Horizon 2020 | en_GB |
dc.description.sponsorship | Volkswagen Foundation | en_GB |
dc.description.sponsorship | Merton College, University of Oxford (NATI) | en_GB |
dc.format.extent | e3002048- | |
dc.format.medium | Electronic-eCollection | |
dc.identifier.citation | Vol. 21(4), article e3002048 | en_GB |
dc.identifier.doi | https://doi.org/10.1371/journal.pbio.3002048 | |
dc.identifier.grantnumber | GBMF5514 | en_GB |
dc.identifier.grantnumber | BB/V008021/1 | en_GB |
dc.identifier.grantnumber | H2020-MSCA-ITN-2015-675752 | en_GB |
dc.identifier.grantnumber | Az 96727 | en_GB |
dc.identifier.uri | http://hdl.handle.net/10871/133065 | |
dc.identifier | ORCID: 0000-0001-9796-1956 (Pagliara, Stefano) | |
dc.identifier | ScopusID: 36641188400 (Pagliara, Stefano) | |
dc.language.iso | en | en_GB |
dc.publisher | Public Library of Science (PLoS) | en_GB |
dc.relation.url | https://www.ncbi.nlm.nih.gov/pubmed/37014915 | en_GB |
dc.relation.url | https://doi.org/10.6084/m9.figshare.22086647 | en_GB |
dc.rights | © 2023 Łapińska et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. | en_GB |
dc.subject | Archaea | en_GB |
dc.subject | Unilamellar Liposomes | en_GB |
dc.subject | Glycerol | en_GB |
dc.subject | Cell Membrane | en_GB |
dc.subject | Bacteria | en_GB |
dc.subject | Membrane Lipids | en_GB |
dc.subject | Phospholipids | en_GB |
dc.subject | Phosphates | en_GB |
dc.subject | Lipid Bilayers | en_GB |
dc.title | Systematic comparison of unilamellar vesicles reveals that archaeal core lipid membranes are more permeable than bacterial membranes | en_GB |
dc.type | Article | en_GB |
dc.date.available | 2023-05-02T10:39:19Z | |
dc.identifier.issn | 1544-9173 | |
exeter.place-of-publication | United States | |
dc.description | This is the final version. Available on open access from the Public Library of Science via the DOI in this record | en_GB |
dc.description | Data Availability: All relevant data are within the paper's Supporting Information files. Numerical values for Fig 4 can be found at https://doi.org/10.6084/m9.figshare.22086647 | en_GB |
dc.identifier.eissn | 1545-7885 | |
dc.identifier.journal | PLoS Biology | en_GB |
dc.relation.ispartof | PLoS Biol, 21(4) | |
dc.rights.uri | https://creativecommons.org/licenses/by/4.0/ | en_GB |
dcterms.dateAccepted | 2023-02-22 | |
dc.rights.license | CC BY | |
rioxxterms.version | VoR | en_GB |
rioxxterms.licenseref.startdate | 2023-04-04 | |
rioxxterms.type | Journal Article/Review | en_GB |
refterms.dateFCD | 2023-05-02T10:36:12Z | |
refterms.versionFCD | VoR | |
refterms.dateFOA | 2023-05-02T10:39:20Z | |
refterms.panel | A | en_GB |
refterms.dateFirstOnline | 2023-04-04 |
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Except where otherwise noted, this item's licence is described as © 2023 Łapińska et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.