Evolution of translation machinery in recoded bacteria enables multi-site incorporation of nonstandard amino acids

Amiram, Miriam; Haimovich, Adrian D.; Fan, Chenguang; Wang, Yane-Shih; Aerni, Hans-Rudolf; Ntai, Ioanna; Moonan, Daniel W.; Ma, Natalie J.; Rovner, Alexis J.; Hong, Seok Hoon; Kelleher, Neil L.; Goodman, Andrew L.; Jewett, Michael C.; Söll, Dieter; Rinehart, Jesse; Isaacs, Farren J.

doi:10.1038/nbt.3372

Title: Evolution of translation machinery in recoded bacteria enables multi-site incorporation of nonstandard amino acids

Journal Article · Mon Nov 16 00:00:00 EST 2015 · Nature Biotechnology

DOI:https://doi.org/10.1038/nbt.3372· OSTI ID:1466973

Amiram, Miriam ^[1]; Haimovich, Adrian D. ^[1]; Fan, Chenguang ^[2];

^[2];

^[3]; Ntai, Ioanna ^[4]; Moonan, Daniel W. ^[1]; Ma, Natalie J. ^[1]; Rovner, Alexis J. ^[1];

^[5]; Kelleher, Neil L. ^[4]; Goodman, Andrew L. ^[6]; Jewett, Michael C. ^[5]; Söll, Dieter ^[7];

^[3]; Isaacs, Farren J. ^[1]

Yale Univ., New Haven, CT (United States). Dept.of Molecular, Cellular, and Developmental Biology and Systems Biology Inst.
Yale Univ., New Haven, CT (United States). Dept. of Molecular Biophysics and Biochemistry
Yale Univ., New Haven, CT (United States). Systems Biology Inst. and Dept. of Cellular and Molecular Physiology
Northwestern Univ., Evanston, IL (United States). Dept. of Chemistry
Northwestern Univ., Evanston, IL (United States). Dept. of Chemical and Biological Engineering
Yale Univ. School of Medicine, New Haven, CT (United States). Dept. of Microbial Pathogenesis and Microbial Sciences Inst.
Yale Univ., New Haven, CT (United States). Dept. of Chemistry and Dept. of Molecular Biophysics and Biochemistry

Expansion of the genetic code with nonstandard amino acids (nsAAs) has enabled biosynthesis of proteins with diverse new chemistries. However, this technology has been largely restricted to proteins containing a single or few nsAA instances. We describe an in vivo evolution approach in a genomically recoded Escherichia coli strain for the selection of orthogonal translation systems capable of multi-site nsAA incorporation. We evolved chromosomal aminoacyl-tRNA synthetases (aaRSs) with up to 25-fold increased protein production for p-acetyl-L-phenylalanine and p-azido-L-phenylalanine (pAzF). We also evolved aaRSs with tunable specificities for 14 nsAAs, including an enzyme that efficiently charges pAzF while excluding 237 other nsAAs. These variants enabled production of elastin-like-polypeptides with 30 nsAA residues at high yields (~50 mg/L) and high accuracy of incorporation (>95%). This approach to aaRS evolution should accelerate and expand our ability to produce functionalized proteins and sequence-defined polymers with diverse chemistries.

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Research Organization:: Harvard Univ., Cambridge, MA (United States)

Sponsoring Organization:: USDOE; Defense Advanced Research Projects Agency (DARPA); National Institutes of Health (NIH); US Army Research Office (ARO); David and Lucile Packard Foundation; Camille Dreyfus Teacher-Scholar Awards Program; Arnold and Mabel Beckman Foundation

Grant/Contract Number:: FG02-02ER63445; N66001-12-C-4020; N66001-12-C-4211; GM22854; GM67193; T32GM007205; 1F30CA196191; W911NF- 11-1-0445

OSTI ID:: 1466973

Journal Information:: Nature Biotechnology, Vol. 33, Issue 12; ISSN 1087-0156

Publisher:: Springer NatureCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 184 works

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CRISPR /Cas9 recombineering‐mediated deep mutational scanning of essential genes in Escherichia coli Choudhury, Alaksh; Fenster, Jacob A.; Fankhauser, Reilly G. Molecular Systems Biology, Vol. 16, Issue 3 https://doi.org/10.15252/msb.20199265	journal	March 2020
Ribosomal frameshifting and transcriptional slippage: From genetic steganography and cryptography to adventitious use. Atkins, John F.; Loughran, Gary; Bhatt, Pramod R. Oxford University Press (OUP) https://doi.org/10.17863/cam.423	journalarticle	January 2016
Computational Aminoacyl-tRNA Synthetase Library Design for Photocaged Tyrosine Baumann, Tobias; Hauf, Matthias; Richter, Florian Humboldt-Universität zu Berlin https://doi.org/10.18452/25460	text	January 2019
Site-Specific Incorporation of Unnatural Amino Acids into Escherichia coli Recombinant Protein: Methodology Development and Recent Achievement Smolskaya, Sviatlana; Andreev, Yaroslav Biomolecules, Vol. 9, Issue 7 https://doi.org/10.3390/biom9070255	journal	June 2019
Escherichia coli Extract-Based Cell-Free Expression System as an Alternative for Difficult-to-Obtain Protein Biosynthesis Smolskaya, Sviatlana; Logashina, Yulia A.; Andreev, Yaroslav A. International Journal of Molecular Sciences, Vol. 21, Issue 3 https://doi.org/10.3390/ijms21030928	journal	January 2020
Intrinsic Properties of tRNA Molecules as Deciphered via Bayesian Network and Distribution Divergence Analysis Branciamore, Sergio; Gogoshin, Grigoriy; Di Giulio, Massimo Life, Vol. 8, Issue 1 https://doi.org/10.3390/life8010005	journal	February 2018
Isolating Escherichia coli strains for recombinant protein production Susan, Schlegel,; Pierre, Genevaux,; Jan-Willem, de Gier, ETH Zurich https://doi.org/10.3929/ethz-b-000121599	text	January 2017

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