Assembly of a unique membrane complex in type VI secretion systems of Bacteroidota

Thibault R. Bongiovanni, Casey J. Latario, Youn Cras, Evan Trus, Sophie Robitaille, Kerry Swartz, Danica Schmidtke, Maxence Vincent, Artemis Kosta, Jan Orth, Florian Stengel, Riccardo Pellarin, Eduardo P. C. Rocha, Benjamin D. Ross () and Eric Durand ()
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Thibault R. Bongiovanni: Institut de Microbiologie, Bioénergies et Biotechnologie (IM2B), Aix-Marseille Université - Centre National de la Recherche Scientifique (CNRS), Unité Mixte de Recherche (UMR) 7255, Institut national de la santé et de la recherche médicale (INSERM)
Casey J. Latario: Geisel School of Medicine at Dartmouth College
Youn Cras: Université Paris Cité, CNRS UMR3525, Microbial Evolutionary Genomics
Evan Trus: Geisel School of Medicine at Dartmouth College
Sophie Robitaille: Geisel School of Medicine at Dartmouth College
Kerry Swartz: Geisel School of Medicine at Dartmouth College
Danica Schmidtke: Geisel School of Medicine at Dartmouth College
Maxence Vincent: Institut de Microbiologie, Bioénergies et Biotechnologie (IM2B), Aix-Marseille Université - Centre National de la Recherche Scientifique (CNRS), Unité Mixte de Recherche (UMR) 7255, Institut national de la santé et de la recherche médicale (INSERM)
Artemis Kosta: Institut de Microbiologie de la Méditerranée (IMM), FR3479, CNRS, Aix-Marseille University
Jan Orth: University of Konstanz, Universitätsstraße 10
Florian Stengel: University of Konstanz, Universitätsstraße 10
Riccardo Pellarin: CNRS & University of Lyon
Eduardo P. C. Rocha: Université Paris Cité, CNRS UMR3525, Microbial Evolutionary Genomics
Benjamin D. Ross: Geisel School of Medicine at Dartmouth College
Eric Durand: Institut de Microbiologie, Bioénergies et Biotechnologie (IM2B), Aix-Marseille Université - Centre National de la Recherche Scientifique (CNRS), Unité Mixte de Recherche (UMR) 7255, Institut national de la santé et de la recherche médicale (INSERM)

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: Abstract The type VI secretion system (T6SS) of Gram-negative bacteria inhibits competitor cells through contact-dependent translocation of toxic effector proteins. In Proteobacteria, the T6SS is anchored to the cell envelope through a megadalton-sized membrane complex (MC). However, the genomes of Bacteroidota with T6SSs appear to lack genes encoding homologs of canonical MC components. Here, we identify five genes in Bacteroides fragilis (tssNQOPR) that are essential for T6SS function and encode a Bacteroidota-specific MC. We purify this complex, reveal its dimensions using electron microscopy, and identify a protein-protein interaction network underlying the assembly of the MC including the stoichiometry of the five TssNQOPR components. Protein TssN mediates the connection between the Bacteroidota MC and the conserved baseplate. Although MC gene content and organization varies across the phylum Bacteroidota, no MC homologs are detected outside of T6SS loci, suggesting ancient co-option and functional convergence with the non-homologous MC of Pseudomonadota.

Date: 2024
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DOI: 10.1038/s41467-023-44426-1

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