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Protein nanowires with tunable functionality and programmable self-assembly using sequence-controlled synthesis

Author

Listed:
  • Daniel Mark Shapiro

    (Yale University
    Yale University
    Yale University
    Yale University)

  • Gunasheil Mandava

    (Yale University
    Yale University)

  • Sibel Ebru Yalcin

    (Yale University
    Yale University)

  • Pol Arranz-Gibert

    (Yale University
    Yale University)

  • Peter J. Dahl

    (Yale University
    Yale University)

  • Catharine Shipps

    (Yale University
    Yale University)

  • Yangqi Gu

    (Yale University
    Yale University)

  • Vishok Srikanth

    (Yale University
    Yale University)

  • Aldo I. Salazar-Morales

    (Yale University
    Yale University)

  • J. Patrick O’Brien

    (Yale University
    Yale University)

  • Koen Vanderschuren

    (Yale University
    Yale University)

  • Dennis Vu

    (Yale University
    Yale University)

  • Victor S. Batista

    (Yale University)

  • Nikhil S. Malvankar

    (Yale University
    Yale University)

  • Farren J. Isaacs

    (Yale University
    Yale University
    Yale University)

Abstract

Advances in synthetic biology permit the genetic encoding of synthetic chemistries at monomeric precision, enabling the synthesis of programmable proteins with tunable properties. Bacterial pili serve as an attractive biomaterial for the development of engineered protein materials due to their ability to self-assemble into mechanically robust filaments. However, most biomaterials lack electronic functionality and atomic structures of putative conductive proteins are not known. Here, we engineer high electronic conductivity in pili produced by a genomically-recoded E. coli strain. Incorporation of tryptophan into pili increased conductivity of individual filaments >80-fold. Computationally-guided ordering of the pili into nanostructures increased conductivity 5-fold compared to unordered pili networks. Site-specific conjugation of pili with gold nanoparticles, facilitated by incorporating the nonstandard amino acid propargyloxy-phenylalanine, increased filament conductivity ~170-fold. This work demonstrates the sequence-defined production of highly-conductive protein nanowires and hybrid organic-inorganic biomaterials with genetically-programmable electronic functionalities not accessible in nature or through chemical-based synthesis.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28206-x
    DOI: 10.1038/s41467-022-28206-x
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    References listed on IDEAS

    as
    1. 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.
    2. Alvaro Alonso-Caballero & Jörg Schönfelder & Simon Poly & Fabiano Corsetti & David Sancho & Emilio Artacho & Raul Perez-Jimenez, 2018. "Mechanical architecture and folding of E. coli type 1 pilus domains," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    3. Harris H. Wang & Farren J. Isaacs & Peter A. Carr & Zachary Z. Sun & George Xu & Craig R. Forest & George M. Church, 2009. "Programming cells by multiplex genome engineering and accelerated evolution," Nature, Nature, vol. 460(7257), pages 894-898, August.
    4. Dongdong Wu & Nairiti Sinha & Jeeyoung Lee & Bryan P. Sutherland & Nicole I. Halaszynski & Yu Tian & Jeffrey Caplan & Huixi Violet Zhang & Jeffery G. Saven & Christopher J. Kloxin & Darrin J. Pochan, 2019. "Polymers with controlled assembly and rigidity made with click-functional peptide bundles," Nature, Nature, vol. 574(7780), pages 658-662, October.
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