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Bidirectional ATP-driven transport of cobalamin by the mycobacterial ABC transporter BacA

Author

Listed:
  • Mark Nijland

    (University of Groningen)

  • Solène N. Lefebvre

    (University of Groningen)

  • Chancievan Thangaratnarajah

    (University of Groningen
    Great Abington)

  • Dirk J. Slotboom

    (University of Groningen)

Abstract

BacA is a mycobacterial ATP-binding cassette (ABC) transporter involved in the translocation of water-soluble compounds across the lipid bilayer. Whole-cell-based assays have shown that BacA imports cobalamin as well as unrelated hydrophilic compounds such as the antibiotic bleomycin and the antimicrobial peptide Bac7 into the cytoplasm. Surprisingly, there are indications that BacA also mediates the export of different antibacterial compounds, which is difficult to reconcile with the notion that ABC transporters generally operate in a strictly unidirectional manner. Here we resolve this conundrum by developing a fluorescence-based transport assay to monitor the transport of cobalamin across liposomal membranes. We find that BacA transports cobalamin in both the import and export direction. This highly unusual bidirectionality suggests that BacA is mechanistically distinct from other ABC transporters and facilitates ATP-driven diffusion, a function that may be important for the evolvability of specific transporters, and may bring competitive advantages to microbial communities.

Suggested Citation

  • Mark Nijland & Solène N. Lefebvre & Chancievan Thangaratnarajah & Dirk J. Slotboom, 2024. "Bidirectional ATP-driven transport of cobalamin by the mycobacterial ABC transporter BacA," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46917-1
    DOI: 10.1038/s41467-024-46917-1
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    References listed on IDEAS

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    1. Nina Grossmann & Ahmet S. Vakkasoglu & Sabine Hulpke & Rupert Abele & Rachelle Gaudet & Robert Tampé, 2014. "Mechanistic determinants of the directionality and energetics of active export by a heterodimeric ABC transporter," Nature Communications, Nature, vol. 5(1), pages 1-10, December.
    2. S. Rempel & E. Colucci & J. W. Gier & A. Guskov & D. J. Slotboom, 2018. "Cysteine-mediated decyanation of vitamin B12 by the predicted membrane transporter BtuM," Nature Communications, Nature, vol. 9(1), pages 1-8, December.
    3. Joris M. H. Goudsmits & Dirk Jan Slotboom & Antoine M. Oijen, 2017. "Single-molecule visualization of conformational changes and substrate transport in the vitamin B12 ABC importer BtuCD-F," Nature Communications, Nature, vol. 8(1), pages 1-10, December.
    4. Lotteke J. Y. M. Swier & Albert Guskov & Dirk J. Slotboom, 2016. "Structural insight in the toppling mechanism of an energy-coupling factor transporter," Nature Communications, Nature, vol. 7(1), pages 1-11, April.
    5. Fabian M. Arnold & Miriam S. Weber & Imre Gonda & Marc J. Gallenito & Sophia Adenau & Pascal Egloff & Iwan Zimmermann & Cedric A. J. Hutter & Lea M. Hürlimann & Eike E. Peters & Jörn Piel & Gabriele M, 2020. "The ABC exporter IrtAB imports and reduces mycobacterial siderophores," Nature, Nature, vol. 580(7803), pages 413-417, April.
    6. S. Rempel & C. Gati & M. Nijland & C. Thangaratnarajah & A. Karyolaimos & J. W. Gier & A. Guskov & D. J. Slotboom, 2020. "A mycobacterial ABC transporter mediates the uptake of hydrophilic compounds," Nature, Nature, vol. 580(7803), pages 409-412, April.
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