Bridges instead of boats? The Mla system of diderm FirmicuteVeillonella parvulareveals an ancestral transenvelope core of phospholipid trafficking Article Swipe
Kyrie P. Grasekamp
,
Basile Beaud
,
Najwa Taïb
,
Bianca Audrain
,
Benjamin Bardiaux
,
Yannick Rossez
,
Nadia Izadi‐Pruneyre
,
Maylis Lejeune
,
Xavier Trivelli
,
Zina Chouit
,
Yann Guérardel
,
Jean‐Marc Ghigo
,
Simonetta Gribaldo
,
Christophe Beloin
·
YOU?
·
· 2023
· Open Access
·
· DOI: https://doi.org/10.1101/2023.06.30.547184
YOU?
·
· 2023
· Open Access
·
· DOI: https://doi.org/10.1101/2023.06.30.547184
Despite extensive characterisation of envelope biogenesis systems in diderm bacteria, glycerophospholipid (GPL) trafficking remains poorly understood, and has only been studied in a handful of model species. Within the Proteobacteria, the maintenance of lipid asymmetry (Mla) system facilitates retrograde GPL trafficking via six proteins, MlaA-F. GPLs are extracted from the outer leaflet of the outer membrane by the lipoprotein MlaA which associates with porin trimers, then shipped through the periplasmic space by the chaperone MlaC, which finally delivers GPLs to the inner membrane complex formed by MlaBDEF. Here, we investigate GPL trafficking in Veillonella parvula , a diderm member of the Firmicutes which encodes an Mla system devoid of MlaA and MlaC. V. parvula Δ mla mutants display phenotypes characteristic of disrupted lipid asymmetry such as hypervesiculation and detergent hypersensitivity, and lipid content analysis from outer membrane vesicles reveals an enrichment for the major lipid component phosphatidylethanolamine. Interestingly, suppressor analysis identifies mutations in tamB that rescue detergent hypersensitivity and hypervesiculation of Δ mla strains, supporting the involvement of these two systems in antagonistic GPL trafficking functions across diverse bacterial lineages. A combination of structural modeling and subcellular localisation assays shows that MlaD Vp is longer than in classical diderm models and forms a transenvelope bridge, encoding both an inner membrane-localised MCE domain and an outer membrane ß-barrel. These results strongly suggest that V. parvula possesses a minimal Mla system for GPL trafficking, replacing the need for chaperones and outer membrane lipoproteins by directly connecting the two membranes. Finally, phylogenomic analysis indicates that this MlaEFD self-contained architecture is widely distributed in diderm bacteria and most likely represents the ancestral functional core of the Mla system, which subsequently increased in complexity in Proteobacteria and closely related phyla following the emergence of MlaABC. Our work broadens the diversity of current models of GPL trafficking in diderm bacteria, challenging the paradigm set by classical models and shedding light on the evolution of a crucial system in the biogenesis and maintenance of the bacterial outer membrane.
Related Topics
Concepts
Bacterial outer membrane
Periplasmic space
Inner membrane
Biology
Biogenesis
Chaperone (clinical)
Porin
Cell biology
Membrane
Chemistry
Biochemistry
Escherichia coli
Gene
Medicine
Pathology
Metadata
- Type
- preprint
- Language
- en
- Landing Page
- https://doi.org/10.1101/2023.06.30.547184
- https://www.biorxiv.org/content/biorxiv/early/2023/06/30/2023.06.30.547184.full.pdf
- OA Status
- green
- References
- 62
- Related Works
- 10
- OpenAlex ID
- https://openalex.org/W4382797223
All OpenAlex metadata
Raw OpenAlex JSON
- OpenAlex ID
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https://openalex.org/W4382797223Canonical identifier for this work in OpenAlex
- DOI
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https://doi.org/10.1101/2023.06.30.547184Digital Object Identifier
- Title
-
Bridges instead of boats? The Mla system of diderm FirmicuteVeillonella parvulareveals an ancestral transenvelope core of phospholipid traffickingWork title
- Type
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preprintOpenAlex work type
- Language
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enPrimary language
- Publication year
-
2023Year of publication
- Publication date
-
2023-06-30Full publication date if available
- Authors
-
Kyrie P. Grasekamp, Basile Beaud, Najwa Taïb, Bianca Audrain, Benjamin Bardiaux, Yannick Rossez, Nadia Izadi‐Pruneyre, Maylis Lejeune, Xavier Trivelli, Zina Chouit, Yann Guérardel, Jean‐Marc Ghigo, Simonetta Gribaldo, Christophe BeloinList of authors in order
- Landing page
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https://doi.org/10.1101/2023.06.30.547184Publisher landing page
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https://www.biorxiv.org/content/biorxiv/early/2023/06/30/2023.06.30.547184.full.pdfDirect link to full text PDF
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YesWhether a free full text is available
- OA status
-
greenOpen access status per OpenAlex
- OA URL
-
https://www.biorxiv.org/content/biorxiv/early/2023/06/30/2023.06.30.547184.full.pdfDirect OA link when available
- Concepts
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Bacterial outer membrane, Periplasmic space, Inner membrane, Biology, Biogenesis, Chaperone (clinical), Porin, Cell biology, Membrane, Chemistry, Biochemistry, Escherichia coli, Gene, Medicine, PathologyTop concepts (fields/topics) attached by OpenAlex
- Cited by
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0Total citation count in OpenAlex
- References (count)
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62Number of works referenced by this work
- Related works (count)
-
10Other works algorithmically related by OpenAlex
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