Evolution of translation machinery in recoded bacteria enables multi-site incorporation of nonstandard amino acids
Abstract
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.
- Authors:
-
- 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
- Publication Date:
- Research Org.:
- Harvard Univ., Cambridge, MA (United States)
- Sponsoring Org.:
- 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
- OSTI Identifier:
- 1466973
- Grant/Contract Number:
- FG02-02ER63445; N66001-12-C-4020; N66001-12-C-4211; GM22854; GM67193; T32GM007205; 1F30CA196191; W911NF- 11-1-0445
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Biotechnology
- Additional Journal Information:
- Journal Volume: 33; Journal Issue: 12; Journal ID: ISSN 1087-0156
- Publisher:
- Springer Nature
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Citation Formats
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, and Isaacs, Farren J. Evolution of translation machinery in recoded bacteria enables multi-site incorporation of nonstandard amino acids. United States: N. p., 2015.
Web. doi:10.1038/nbt.3372.
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. Evolution of translation machinery in recoded bacteria enables multi-site incorporation of nonstandard amino acids. United States. https://doi.org/10.1038/nbt.3372
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, and Isaacs, Farren J. Mon .
"Evolution of translation machinery in recoded bacteria enables multi-site incorporation of nonstandard amino acids". United States. https://doi.org/10.1038/nbt.3372. https://www.osti.gov/servlets/purl/1466973.
@article{osti_1466973,
title = {Evolution of translation machinery in recoded bacteria enables multi-site incorporation of nonstandard amino acids},
author = {Amiram, Miriam and Haimovich, Adrian D. and Fan, Chenguang and Wang, Yane-Shih and Aerni, Hans-Rudolf and Ntai, Ioanna and Moonan, Daniel W. and Ma, Natalie J. and Rovner, Alexis J. and Hong, Seok Hoon and Kelleher, Neil L. and Goodman, Andrew L. and Jewett, Michael C. and Söll, Dieter and Rinehart, Jesse and Isaacs, Farren J.},
abstractNote = {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.},
doi = {10.1038/nbt.3372},
journal = {Nature Biotechnology},
number = 12,
volume = 33,
place = {United States},
year = {Mon Nov 16 00:00:00 EST 2015},
month = {Mon Nov 16 00:00:00 EST 2015}
}
Web of Science
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- Acevedo-Rocha, Carlos G.; Budisa, Nediljko
- Microbial Biotechnology, Vol. 9, Issue 5
CRISPR /Cas9 recombineering‐mediated deep mutational scanning of essential genes in Escherichia coli
journal, March 2020
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A Plasmid Set for Efficient Bacterial Artificial Chromosome (BAC) Transgenesis in Zebrafish
journal, January 2016
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Ribosomal frameshifting and transcriptional slippage: From genetic steganography and cryptography to adventitious use.
journalarticle, January 2016
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- Oxford University Press (OUP)
Computational Aminoacyl-tRNA Synthetase Library Design for Photocaged Tyrosine
text, January 2019
- Baumann, Tobias; Hauf, Matthias; Richter, Florian
- Humboldt-Universität zu Berlin
Site-Specific Incorporation of Unnatural Amino Acids into Escherichia coli Recombinant Protein: Methodology Development and Recent Achievement
journal, June 2019
- Smolskaya, Sviatlana; Andreev, Yaroslav
- Biomolecules, Vol. 9, Issue 7
Dissecting the Contribution of Release Factor Interactions to Amber Stop Codon Reassignment Efficiencies of the Methanocaldococcus jannaschii Orthogonal Pair
journal, November 2018
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Translational Control using an Expanded Genetic Code
journal, February 2019
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Aminoacyl-tRNA Synthetases and tRNAs for an Expanded Genetic Code: What Makes them Orthogonal?
journal, April 2019
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Plasticity and Constraints of tRNA Aminoacylation Define Directed Evolution of Aminoacyl-tRNA Synthetases
journal, May 2019
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- International Journal of Molecular Sciences, Vol. 20, Issue 9
Escherichia coli Extract-Based Cell-Free Expression System as an Alternative for Difficult-to-Obtain Protein Biosynthesis
journal, January 2020
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Intrinsic Properties of tRNA Molecules as Deciphered via Bayesian Network and Distribution Divergence Analysis
journal, February 2018
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The Role of Orthogonality in Genetic Code Expansion
journal, July 2019
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Isolating Escherichia coli strains for recombinant protein production
text, January 2017
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- ETH Zurich