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The translocation assembly module (TAM) catalyzes the assembly of bacterial outer membrane proteins in vitro

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  • Xu Wang

    (National Institutes of Health)

  • Sarah B. Nyenhuis

    (National Institutes of Health)

  • Harris D. Bernstein

    (National Institutes of Health)

Abstract

The translocation and assembly module (TAM) has been proposed to play a crucial role in the assembly of a small subset of outer membrane proteins (OMPs) in Proteobacteria based on experiments conducted in vivo using tamA and tamB mutant strains and in vitro using biophysical methods. TAM consists of an OMP (TamA) and a periplasmic protein that is anchored to the inner membrane by a single α helix (TamB). Here we examine the function of the purified E. coli complex in vitro after reconstituting it into proteoliposomes. We find that TAM catalyzes the assembly of four model OMPs nearly as well as the β-barrel assembly machine (BAM), a universal heterooligomer that contains a TamA homolog (BamA) and that catalyzes the assembly of almost all E. coli OMPs. Consistent with previous results, both TamA and TamB are required for significant TAM activity. Our study provides direct evidence that TAM can function as an independent OMP insertase and describes a new method to gain insights into TAM function.

Suggested Citation

  • Xu Wang & Sarah B. Nyenhuis & Harris D. Bernstein, 2024. "The translocation assembly module (TAM) catalyzes the assembly of bacterial outer membrane proteins in vitro," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51628-8
    DOI: 10.1038/s41467-024-51628-8
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    1. Nicholas Noinaj & Adam J. Kuszak & James C. Gumbart & Petra Lukacik & Hoshing Chang & Nicole C. Easley & Trevor Lithgow & Susan K. Buchanan, 2013. "Structural insight into the biogenesis of β-barrel membrane proteins," Nature, Nature, vol. 501(7467), pages 385-390, September.
    2. Hironori Takeda & Akihisa Tsutsumi & Tomohiro Nishizawa & Caroline Lindau & Jon V. Busto & Lena-Sophie Wenz & Lars Ellenrieder & Kenichiro Imai & Sebastian P. Straub & Waltraut Mossmann & Jian Qiu & Y, 2021. "Mitochondrial sorting and assembly machinery operates by β-barrel switching," Nature, Nature, vol. 590(7844), pages 163-169, February.
    3. Tobias Krojer & Justyna Sawa & Eva Schäfer & Helen R. Saibil & Michael Ehrmann & Tim Clausen, 2008. "Structural basis for the regulated protease and chaperone function of DegP," Nature, Nature, vol. 453(7197), pages 885-890, June.
    4. Rakesh Sikdar & Janine H. Peterson & D. Eric Anderson & Harris D. Bernstein, 2017. "Folding of a bacterial integral outer membrane protein is initiated in the periplasm," Nature Communications, Nature, vol. 8(1), pages 1-12, December.
    5. Parthasarathi Rath & Adrian Hermann & Ramona Schaefer & Elia Agustoni & Jean-Marie Vonach & Martin Siegrist & Christian Miscenic & Andreas Tschumi & Doris Roth & Christoph Bieniossek & Sebastian Hille, 2023. "High-throughput screening of BAM inhibitors in native membrane environment," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    6. Yu Imai & Kirsten J. Meyer & Akira Iinishi & Quentin Favre-Godal & Robert Green & Sylvie Manuse & Mariaelena Caboni & Miho Mori & Samantha Niles & Meghan Ghiglieri & Chandrashekhar Honrao & Xiaoyu Ma , 2019. "A new antibiotic selectively kills Gram-negative pathogens," Nature, Nature, vol. 576(7787), pages 459-464, December.
    7. Hsin-Hui Shen & Denisse L. Leyton & Takuya Shiota & Matthew J. Belousoff & Nicholas Noinaj & Jingxiong Lu & Stephen A. Holt & Khershing Tan & Joel Selkrig & Chaille T. Webb & Susan K. Buchanan & Lisan, 2014. "Reconstitution of a nanomachine driving the assembly of proteins into bacterial outer membranes," Nature Communications, Nature, vol. 5(1), pages 1-10, December.
    8. Matthew T. Doyle & Harris D. Bernstein, 2019. "Bacterial outer membrane proteins assemble via asymmetric interactions with the BamA β-barrel," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    9. Mu Gao & Davi Nakajima An & Jerry M. Parks & Jeffrey Skolnick, 2022. "AF2Complex predicts direct physical interactions in multimeric proteins with deep learning," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    10. Hundeep Kaur & Roman P. Jakob & Jan K. Marzinek & Robert Green & Yu Imai & Jani Reddy Bolla & Elia Agustoni & Carol V. Robinson & Peter J. Bond & Kim Lewis & Timm Maier & Sebastian Hiller, 2021. "The antibiotic darobactin mimics a β-strand to inhibit outer membrane insertase," Nature, Nature, vol. 593(7857), pages 125-129, May.
    11. Yinghong Gu & Huanyu Li & Haohao Dong & Yi Zeng & Zhengyu Zhang & Neil G. Paterson & Phillip J. Stansfeld & Zhongshan Wang & Yizheng Zhang & Wenjian Wang & Changjiang Dong, 2016. "Structural basis of outer membrane protein insertion by the BAM complex," Nature, Nature, vol. 531(7592), pages 64-69, March.
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