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Chapter 9 : The TAM: A Translocation and Assembly Module of the β-barrel Assembly Machinery in Bacterial Outer Membranes

Authors: Christopher J. Stubenrauch, Trevor Lithgow
Content Type: Monograph
Publication Year: 2019

Category: Bacterial Pathogenesis

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The TAM: A Translocation and Assembly Module of the β-barrel Assembly Machinery in Bacterial Outer Membranes, Page 1 of 2

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Abstract:

The vast majority of integral membrane proteins residing within the outer membrane of Gram-negative bacteria adopt a β-barrel architecture. Mechanistically, how these proteins fold remains uncertain, but the process requires assistance from at least two nanomachines: the translocation and assembly module (TAM) and the β-barrel assembly machinery (BAM) complex ( ). But whether the TAM and the BAM complex collaborate or act independently on each nascent membrane protein substrate arriving at the outer membrane has yet to be determined. The TAM is comprised of two subunits: TamA, an integral outer membrane protein ( ), and TamB, an inner membrane-anchored protein ( ). The BAM complex is variable in composition between genera, and it is comprised of 2 to 5 accessory lipoproteins attached to an integral outer membrane protein, BamA ( ).

Citation: Stubenrauch C, Lithgow T. 2019. The TAM: A Translocation and Assembly Module of the β-barrel Assembly Machinery in Bacterial Outer Membranes, p 103-111. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/ecosalplus.ESP-0036-2018
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The TAM: A Translocation and Assembly Module of the β-barrel Assembly Machinery in Bacterial Outer Membranes
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Citation: Stubenrauch C, Lithgow T. 2019. The TAM: A Translocation and Assembly Module of the β-barrel Assembly Machinery in Bacterial Outer Membranes, p 103-111. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/ecosalplus.ESP-0036-2018
/content/10.1128/9781683670285.chap9.fig9-1
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 ( ), 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 ( ), 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 ( ). Residue numbers are indicated above (first residue) and below (last residue) the domain in question.
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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 ( ), 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 ( ), 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 ( ). 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, p 103-111. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/ecosalplus.ESP-0036-2018
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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. ( ).
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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. ( ).

Citation: Stubenrauch C, Lithgow T. 2019. The TAM: A Translocation and Assembly Module of the β-barrel Assembly Machinery in Bacterial Outer Membranes, p 103-111. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/ecosalplus.ESP-0036-2018
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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 ( ). 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.
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10.1128/9781683670285/fig9-3.gif
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 ( ). 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, p 103-111. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/ecosalplus.ESP-0036-2018
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