The Mla system of diderm Firmicute Veillonella parvula reveals an ancestral transenvelope bridge for phospholipid trafficking

Kyrie P. Grasekamp, Basile Beaud Benyahia, Najwa Taib, Bianca Audrain, Benjamin Bardiaux, Yannick Rossez, Nadia Izadi-Pruneyre, Maylis Lejeune, Xavier Trivelli, Zina Chouit, Yann Guerardel, Jean-Marc Ghigo, Simonetta Gribaldo () and Christophe Beloin ()
Additional contact information
Kyrie P. Grasekamp: Université Paris Cité, Genetics of Biofilms Laboratory
Basile Beaud Benyahia: Université Paris Cité, Evolutionary Biology of the Microbial Cell Laboratory
Najwa Taib: Université Paris Cité, Evolutionary Biology of the Microbial Cell Laboratory
Bianca Audrain: Université Paris Cité, Genetics of Biofilms Laboratory
Benjamin Bardiaux: Université Paris Cité, Structural Bioinformatics Unit, CNRS UMR 3528
Yannick Rossez: Université de Lille, CNRS, UMR 8576 – UGSF – Unité de Glycobiologie Structurale et Fonctionnelle
Nadia Izadi-Pruneyre: Université Paris Cité, Structural Bioinformatics Unit, CNRS UMR 3528
Maylis Lejeune: Université Paris Cité, Structural Bioinformatics Unit, CNRS UMR 3528
Xavier Trivelli: Université de Lille, CNRS, INRAE, Centrale Lille, Université d’Artois, FR 2638 − IMEC − Institut Michel-Eugène Chevreul
Zina Chouit: Université de Lille, CNRS, UMR 8576 – UGSF – Unité de Glycobiologie Structurale et Fonctionnelle
Yann Guerardel: Université de Lille, CNRS, UMR 8576 – UGSF – Unité de Glycobiologie Structurale et Fonctionnelle
Jean-Marc Ghigo: Université Paris Cité, Genetics of Biofilms Laboratory
Simonetta Gribaldo: Université Paris Cité, Evolutionary Biology of the Microbial Cell Laboratory
Christophe Beloin: Université Paris Cité, Genetics of Biofilms Laboratory

Nature Communications, 2023, vol. 14, issue 1, 1-15

Abstract: Abstract E. coli and most other diderm bacteria (those with two membranes) have an inner membrane enriched in glycerophospholipids (GPLs) and an asymmetric outer membrane (OM) containing GPLs in its inner leaflet and primarily lipopolysaccharides in its outer leaflet. In E. coli, this lipid asymmetry is maintained by the Mla system which consists of six proteins: the OM lipoprotein MlaA extracts GPLs from the outer leaflet, and the periplasmic chaperone MlaC transfers them across the periplasm to the inner membrane complex MlaBDEF. However, GPL trafficking still remains poorly understood, and has only been studied in a handful of model species. Here, we investigate GPL trafficking in Veillonella parvula, a diderm Firmicute with an Mla system that lacks MlaA and MlaC, but contains an elongated MlaD. V. parvula mla mutants display phenotypes characteristic of disrupted lipid asymmetry which can be suppressed by mutations in tamB, supporting that these two systems have opposite GPL trafficking functions across diverse bacterial lineages. Structural modelling and subcellular localisation assays suggest that V. parvula MlaD forms a transenvelope bridge, comprising a typical inner membrane-localised MCE domain and, in addition, an outer membrane ß-barrel. Phylogenomic analyses indicate that this elongated MlaD type is widely distributed across diderm bacteria and likely forms part of the ancestral functional core of the Mla system, which would be composed of MlaEFD only.

Date: 2023
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DOI: 10.1038/s41467-023-43411-y

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