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Domain 4:

Synthesis and Processing of Macromolecules

The TAM: A Translocation and Assembly Module of the β-Barrel Assembly Machinery in Bacterial Outer Membranes

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  • Authors: Christopher J. Stubenrauch1, and Trevor Lithgow2
  • Editors: Maria Sandkvist3, Eric Cascales4, Peter J. Christie5
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Infection & Immunity Program, Biomedicine Discovery Institute, and Department of Microbiology, Monash University, Clayton 3800, Australia; 2: Infection & Immunity Program, Biomedicine Discovery Institute, and Department of Microbiology, Monash University, Clayton 3800, Australia; 3: Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan; 4: CNRS Aix-Marseille Université, Mediterranean Institute of Microbiology, Marseille, France; 5: Department of Microbiology and Molecular Genetics, McGovern Medical School, Houston, Texas
  • Received 21 August 2018 Accepted 18 December 2018 Published 27 February 2019
  • Address correspondence to Trevor Lithgow, [email protected]edu
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  • Abstract:

    Assembly of proteins into the outer membrane is an essential process in the cell biology of bacteria. The integration of β-barrel proteins into the outer membrane is mediated by a system referred to as the β-barrel assembly machinery (BAM) that includes two related proteins: BamA in the BAM complex and TamA in the TAM (translocation and assembly module). Here we review what is known about the TAM in terms of its function and the structural architecture of its two subunits, TamA and TamB. By linking the energy transduction possibilities in the inner membrane to TamA in the outer membrane, the TAM provides additional capability to the β-barrel assembly machinery. Conservation of the TAM across evolutionary boundaries, and the presence of hybrid BAM/TAM complexes in some bacterial lineages, adds insight to our growing understanding of how bacterial outer membranes are built.

  • Citation: Stubenrauch C, Lithgow T. 2019. The TAM: A Translocation and Assembly Module of the β-Barrel Assembly Machinery in Bacterial Outer Membranes, EcoSal Plus 2019; doi:10.1128/ecosalplus.ESP-0036-2018

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/content/journal/ecosalplus/10.1128/ecosalplus.ESP-0036-2018
2019-02-27
2019-03-23

Abstract:

Assembly of proteins into the outer membrane is an essential process in the cell biology of bacteria. The integration of β-barrel proteins into the outer membrane is mediated by a system referred to as the β-barrel assembly machinery (BAM) that includes two related proteins: BamA in the BAM complex and TamA in the TAM (translocation and assembly module). Here we review what is known about the TAM in terms of its function and the structural architecture of its two subunits, TamA and TamB. By linking the energy transduction possibilities in the inner membrane to TamA in the outer membrane, the TAM provides additional capability to the β-barrel assembly machinery. Conservation of the TAM across evolutionary boundaries, and the presence of hybrid BAM/TAM complexes in some bacterial lineages, adds insight to our growing understanding of how bacterial outer membranes are built.

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Figures

Image of Figure 1
Figure 1

Nascent TamA contains a signal peptide (SP) that is cleaved during translocation across the inner membrane (IM). The mature protein comprises residues 22 to 577 ( 2 ), with three POTRA domains (numbered from the N terminus) connected to a 16-stranded β-barrel. (Left) Domain distribution of TamA showing the protein data bank (pdb) entries for the five solved structures and their respective amino acid coverage. (Right) A ribbon diagram of the full-length TamA (pdb code 4c00). TamB is tethered to the IM through an IM anchor, but the bulk of the protein resides within the periplasm. (Bottom) A ribbon diagram of the solved structure of TamB with its pdb code indicated. Using the Phyre2 homology server ( 31 ), additional structures were determined as shown by modeling the remaining region of TamB on the solved structure. (Top) The domain distribution of TamB with the confidence in the predicted structures indicated, as determined by the Phyre2 homology server ( 31 ). Residue numbers are indicated above (first residue) and below (last residue) the domain in question.

Citation: Stubenrauch C, Lithgow T. 2019. The TAM: A Translocation and Assembly Module of the β-Barrel Assembly Machinery in Bacterial Outer Membranes, EcoSal Plus 2019; doi:10.1128/ecosalplus.ESP-0036-2018
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Image of Figure 2
Figure 2

Ribbon diagram and surface structures of TamA (pdb code 4c00). Interstrand hydrogen bonding (yellow dashed lines) within the TamA β-barrel is prominent between all strands, except the first and last strands that form the lateral gate (shown in purple), where only 2 hydrogen bonds are observed. Inset, close-up view of the hydrogen bonding network involving the main chain atoms of the first and last strands, where the atoms are colored as follows: C, gray; H, white; N, blue; and O, red. Aromatic residues within the β-barrel are shown in pink, and the likely positions of the lipid head groups at, or opposite, the lateral gate (shown in purple) are indicated by black dashed lines. The distances between the dashed lines are as per Selkrig et al. ( 27 ).

Citation: Stubenrauch C, Lithgow T. 2019. The TAM: A Translocation and Assembly Module of the β-Barrel Assembly Machinery in Bacterial Outer Membranes, EcoSal Plus 2019; doi:10.1128/ecosalplus.ESP-0036-2018
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Image of Figure 3
Figure 3

For the purpose of clarity, the BAM complex is not shown. As noted in the text, it remains unclear whether the TAM and the BAM complex collaborate or act independently on each molecule of their outer membrane protein substrates. A substrate is translocated across the inner membrane (IM) via the Sec translocon. The TAM is in a substrate-ready conformation, where the structural features of the TamA β-barrel (highlighted in Fig. 2 ) cause membrane thinning and increased lipid disorder near the TamA lateral gate. The substrate makes its way across the periplasm and engages the TAM. This causes a structural change in TamA, whereby its POTRA domains extend 33 Å from the β-barrel domain ( 27 , 32 ). TamB is rigidified by the peptidoglycan (PG) layer and the turgor pressure of the IM, so the movement of the POTRA domains causes a local raising of the outer membrane (OM) that increases lipid disorder and lowers the activation energy required for substrate insertion. The substrate passes through the lumen of TamA and uses the β-strands comprising the TamA lateral gate as a template to fold into a β-barrel itself. The substrate is released into the OM, allowing the POTRA domains to retract 33 Å so that the TAM is reset into its substrate-ready conformation.

Citation: Stubenrauch C, Lithgow T. 2019. The TAM: A Translocation and Assembly Module of the β-Barrel Assembly Machinery in Bacterial Outer Membranes, EcoSal Plus 2019; doi:10.1128/ecosalplus.ESP-0036-2018
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