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Structure of Geobacter pili reveals secretory rather than nanowire behaviour

Author

Listed:
  • Yangqi Gu

    (Microbial Sciences Institute Yale University
    Yale University)

  • Vishok Srikanth

    (Microbial Sciences Institute Yale University
    Yale University)

  • Aldo I. Salazar-Morales

    (Microbial Sciences Institute Yale University
    Yale University)

  • Ruchi Jain

    (Microbial Sciences Institute Yale University
    Yale University)

  • J. Patrick O’Brien

    (Microbial Sciences Institute Yale University
    Yale University)

  • Sophia M. Yi

    (Microbial Sciences Institute Yale University
    Yale University)

  • Rajesh Kumar Soni

    (Proteomics and Macromolecular Crystallography Shared Resource, Herbert Irving Comprehensive Cancer Center, Columbia University Irving Medical Center)

  • Fadel A. Samatey

    (Microbial Sciences Institute Yale University
    Yale University)

  • Sibel Ebru Yalcin

    (Microbial Sciences Institute Yale University
    Yale University)

  • Nikhil S. Malvankar

    (Microbial Sciences Institute Yale University
    Yale University)

Abstract

Extracellular electron transfer by Geobacter species through surface appendages known as microbial nanowires1 is important in a range of globally important environmental phenomena2, as well as for applications in bio-remediation, bioenergy, biofuels and bioelectronics. Since 2005, these nanowires have been thought to be type 4 pili composed solely of the PilA-N protein1. However, previous structural analyses have demonstrated that, during extracellular electron transfer, cells do not produce pili but rather nanowires made up of the cytochromes OmcS2,3 and OmcZ4. Here we show that Geobacter sulfurreducens binds PilA-N to PilA-C to assemble heterodimeric pili, which remain periplasmic under nanowire-producing conditions that require extracellular electron transfer5. Cryo-electron microscopy revealed that C-terminal residues of PilA-N stabilize its copolymerization with PilA-C (to form PilA-N–C) through electrostatic and hydrophobic interactions that position PilA-C along the outer surface of the filament. PilA-N–C filaments lack π-stacking of aromatic side chains and show a conductivity that is 20,000-fold lower than that of OmcZ nanowires. In contrast with surface-displayed type 4 pili, PilA-N–C filaments show structure, function and localization akin to those of type 2 secretion pseudopili6. The secretion of OmcS and OmcZ nanowires is lost when pilA-N is deleted and restored when PilA-N–C filaments are reconstituted. The substitution of pilA-N with the type 4 pili of other microorganisms also causes a loss of secretion of OmcZ nanowires. As all major phyla of prokaryotes use systems similar to type 4 pili, this nanowire translocation machinery may have a widespread effect in identifying the evolution and prevalence of diverse electron-transferring microorganisms and in determining nanowire assembly architecture for designing synthetic protein nanowires.

Suggested Citation

  • Yangqi Gu & Vishok Srikanth & Aldo I. Salazar-Morales & Ruchi Jain & J. Patrick O’Brien & Sophia M. Yi & Rajesh Kumar Soni & Fadel A. Samatey & Sibel Ebru Yalcin & Nikhil S. Malvankar, 2021. "Structure of Geobacter pili reveals secretory rather than nanowire behaviour," Nature, Nature, vol. 597(7876), pages 430-434, September.
  • Handle: RePEc:nat:nature:v:597:y:2021:i:7876:d:10.1038_s41586-021-03857-w
    DOI: 10.1038/s41586-021-03857-w
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    Citations

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    Cited by:

    1. Heleen T. Ouboter & Rob Mesman & Tom Sleutels & Jelle Postma & Martijn Wissink & Mike S. M. Jetten & Annemiek Ter Heijne & Tom Berben & Cornelia U. Welte, 2024. "Mechanisms of extracellular electron transfer in anaerobic methanotrophic archaea," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    2. Daniel Mark Shapiro & Gunasheil Mandava & Sibel Ebru Yalcin & Pol Arranz-Gibert & Peter J. Dahl & Catharine Shipps & Yangqi Gu & Vishok Srikanth & Aldo I. Salazar-Morales & J. Patrick O’Brien & Koen V, 2022. "Protein nanowires with tunable functionality and programmable self-assembly using sequence-controlled synthesis," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    3. Robin Anger & Laetitia Pieulle & Meriam Shahin & Odile Valette & Hugo Guenno & Artemis Kosta & Vladimir Pelicic & Rémi Fronzes, 2023. "Structure of a heteropolymeric type 4 pilus from a monoderm bacterium," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    4. Matteo Tassinari & Marta Rudzite & Alain Filloux & Harry H. Low, 2023. "Assembly mechanism of a Tad secretion system secretin-pilotin complex," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    5. Jens Neu & Catharine C. Shipps & Matthew J. Guberman-Pfeffer & Cong Shen & Vishok Srikanth & Jacob A. Spies & Nathan D. Kirchhofer & Sibel Ebru Yalcin & Gary W. Brudvig & Victor S. Batista & Nikhil S., 2022. "Microbial biofilms as living photoconductors due to ultrafast electron transfer in cytochrome OmcS nanowires," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    6. Pilar C. Portela & Catharine C. Shipps & Cong Shen & Vishok Srikanth & Carlos A. Salgueiro & Nikhil S. Malvankar, 2024. "Widespread extracellular electron transfer pathways for charging microbial cytochrome OmcS nanowires via periplasmic cytochromes PpcABCDE," Nature Communications, Nature, vol. 15(1), pages 1-13, December.

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