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Title: Natural separation of the acyl-CoA ligase reaction results in a non-adenylating enzyme

Abstract

Acyl-coenzyme A (CoA) ligases catalyze the activation of carboxylic acids via a two-step reaction of adenylation followed by thioesterification. Here, we report the discovery of a non-adenylating acyl-CoA ligase PtmA2 and the functional separation of an acyl-CoA ligase reaction. Both PtmA1 and PtmA2, two acyl-CoA ligases from the biosynthetic pathway of platensimycin and platencin, are necessary for the two steps of CoA activation. Gene inactivation of ptmA1 and ptmA2 resulted in the accumulation of free acid and adenylate intermediates, respectively. Enzymatic and structural characterization of PtmA2 confirmed its ability to only catalyze thioesterification. Structural characterization of PtmA2 revealed it binds both free acid and adenylate substrates and undergoes the established mechanism of domain alternation. Finally, site-directed mutagenesis restored both the adenylation and complete CoA activation reactions. This study challenges the currently accepted paradigm of adenylating enzymes and inspires future investigations on functionally separated acyl-CoA ligases and their ramifications in biology.

Authors:
 [1]; ORCiD logo [1]; ORCiD logo [1];  [2];  [2];  [2];  [1];  [2];  [2];  [3]; ORCiD logo [4]
+ Show Author Affiliations
  1. Scripps Research Inst., Jupiter, FL (United States). Dept. of Chemistry
  2. Argonne National Lab. (ANL), Argonne, IL (United States). Midwest Center for Structural Genomics and Structural Biology Center, Biosciences Division
  3. Rice Univ., Houston, TX (United States). Dept. of Biosciences
  4. Scripps Research Inst., Jupiter, FL (United States). Dept. of Chemistry; Scripps Research Inst., Jupiter, FL (United States). Dept of Molecular Medicine; Scripps Research Inst., Jupiter, FL (United States). Natural Products Library Initiative at The Scripps Research Inst.
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH); Chinese Academy of Sciences (CAS); Arnold and Mabel Beckman Foundation
OSTI Identifier:
1466308
Grant/Contract Number:  
AC02-06CH11357; GM094585; GM098248; GM109456; GM114353
Resource Type:
Accepted Manuscript
Journal Name:
Nature Chemical Biology
Additional Journal Information:
Journal Volume: 14; Journal Issue: 7; Journal ID: ISSN 1552-4450
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Wang, Nan, Rudolf, Jeffrey D., Dong, Liao-Bin, Osipiuk, Jerzy, Hatzos-Skintges, Catherine, Endres, Michael, Chang, Chin-Yuan, Babnigg, Gyorgy, Joachimiak, Andrzej, Phillips, George N., and Shen, Ben. Natural separation of the acyl-CoA ligase reaction results in a non-adenylating enzyme. United States: N. p., 2018. Web. doi:10.1038/s41589-018-0061-0.
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Wang, Nan, Rudolf, Jeffrey D., Dong, Liao-Bin, Osipiuk, Jerzy, Hatzos-Skintges, Catherine, Endres, Michael, Chang, Chin-Yuan, Babnigg, Gyorgy, Joachimiak, Andrzej, Phillips, George N., & Shen, Ben. Natural separation of the acyl-CoA ligase reaction results in a non-adenylating enzyme. United States. https://doi.org/10.1038/s41589-018-0061-0
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Wang, Nan, Rudolf, Jeffrey D., Dong, Liao-Bin, Osipiuk, Jerzy, Hatzos-Skintges, Catherine, Endres, Michael, Chang, Chin-Yuan, Babnigg, Gyorgy, Joachimiak, Andrzej, Phillips, George N., and Shen, Ben. Mon . "Natural separation of the acyl-CoA ligase reaction results in a non-adenylating enzyme". United States. https://doi.org/10.1038/s41589-018-0061-0. https://www.osti.gov/servlets/purl/1466308.
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@article{osti_1466308,
title = {Natural separation of the acyl-CoA ligase reaction results in a non-adenylating enzyme},
author = {Wang, Nan and Rudolf, Jeffrey D. and Dong, Liao-Bin and Osipiuk, Jerzy and Hatzos-Skintges, Catherine and Endres, Michael and Chang, Chin-Yuan and Babnigg, Gyorgy and Joachimiak, Andrzej and Phillips, George N. and Shen, Ben},
abstractNote = {Acyl-coenzyme A (CoA) ligases catalyze the activation of carboxylic acids via a two-step reaction of adenylation followed by thioesterification. Here, we report the discovery of a non-adenylating acyl-CoA ligase PtmA2 and the functional separation of an acyl-CoA ligase reaction. Both PtmA1 and PtmA2, two acyl-CoA ligases from the biosynthetic pathway of platensimycin and platencin, are necessary for the two steps of CoA activation. Gene inactivation of ptmA1 and ptmA2 resulted in the accumulation of free acid and adenylate intermediates, respectively. Enzymatic and structural characterization of PtmA2 confirmed its ability to only catalyze thioesterification. Structural characterization of PtmA2 revealed it binds both free acid and adenylate substrates and undergoes the established mechanism of domain alternation. Finally, site-directed mutagenesis restored both the adenylation and complete CoA activation reactions. This study challenges the currently accepted paradigm of adenylating enzymes and inspires future investigations on functionally separated acyl-CoA ligases and their ramifications in biology.},
doi = {10.1038/s41589-018-0061-0},
journal = {Nature Chemical Biology},
number = 7,
volume = 14,
place = {United States},
year = {2018},
month = {6}
}
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https://doi.org/10.1038/s41589-018-0061-0
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Titer improvement and pilot-scale production of platensimycin from Streptomyces platensis SB12026
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A general introduction to the biochemistry of mitochondrial fatty acid β-oxidation
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Antibacterial sulfur-containing platensimycin and platencin congeners from Streptomyces platensis SB12029
journal, December 2016

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In vivo instability of platensimycin and platencin: Synthesis and biological evaluation of urea- and carbamate-platensimycin
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Structural and Functional Studies of Fatty Acyl Adenylate Ligases from E. coli and L. pneumophila
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Molecular Basis of the Functional Divergence of Fatty Acyl-AMP Ligase Biosynthetic Enzymes of Mycobacterium tuberculosis
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Adenylate-forming enzymes
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Characterization of the Propionyl-CoA Synthetase (PrpE) Enzyme of Salmonella enterica :  Residue Lys592 Is Required for Propionyl-AMP Synthesis †
journal, February 2002

  • Horswill, Alexander R.; Escalante-Semerena, Jorge C.
  • Biochemistry, Vol. 41, Issue 7
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The 1.75 Å Crystal Structure of Acetyl-CoA Synthetase Bound to Adenosine-5‘-propylphosphate and Coenzyme A †
journal, March 2003

  • Gulick, Andrew M.; Starai, Vincent J.; Horswill, Alexander R.
  • Biochemistry, Vol. 42, Issue 10, p. 2866-2873
  • DOI: 10.1021/bi0271603

Crystal Structure of 4-Chlorobenzoate:CoA Ligase/Synthetase in the Unliganded and Aryl Substrate-Bound States † , ‡
journal, July 2004

  • Gulick, Andrew M.; Lu, Xuefeng; Dunaway-Mariano, Debra
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  • DOI: 10.1021/bi049384m

Mechanism of 4-Chlorobenzoate:Coenzyme A Ligase Catalysis †
journal, August 2008

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journal, May 2009

  • Wu, Rui; Reger, Albert S.; Lu, Xuefeng
  • Biochemistry, Vol. 48, Issue 19
  • DOI: 10.1021/bi9002327

Conformational Dynamics in the Acyl-CoA Synthetases, Adenylation Domains of Non-ribosomal Peptide Synthetases, and Firefly Luciferase
journal, October 2009

  • Gulick, Andrew M.
  • ACS Chemical Biology, Vol. 4, Issue 10, p. 811-827
  • DOI: 10.1021/cb900156h

Modular Peptide Synthetases Involved in Nonribosomal Peptide Synthesis
journal, November 1997

  • Marahiel, Mohamed A.; Stachelhaus, Torsten; Mootz, Henning D.
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Expression of the Platencin Biosynthetic Gene Cluster in Heterologous Hosts Yielding New Platencin Congeners
journal, November 2012

  • Smanski, Michael J.; Casper, Jeffrey; Peterson, Ryan M.
  • Journal of Natural Products, Vol. 75, Issue 12
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Strain Prioritization for Natural Product Discovery by a High-Throughput Real-Time PCR Method
journal, September 2014

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Enzymic activation and transfer of fatty acids as acyl-adenylates in mycobacteria
journal, March 2004

  • Trivedi, Omita A.; Arora, Pooja; Sridharan, Vijayalakshmi
  • Nature, Vol. 428, Issue 6981
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Mechanistic and functional insights into fatty acid activation in Mycobacterium tuberculosis
journal, February 2009

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  • Nature Chemical Biology, Vol. 5, Issue 3
  • DOI: 10.1038/nchembio.143

The pimeloyl-CoA synthetase BioW defines a new fold for adenylate-forming enzymes
journal, April 2017

  • Estrada, Paola; Manandhar, Miglena; Dong, Shi-Hui
  • Nature Chemical Biology, Vol. 13, Issue 6
  • DOI: 10.1038/nchembio.2359

PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin
journal, January 2003

  • Gust, B.; Challis, G. L.; Fowler, K.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 4
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Reversible lysine acetylation controls the activity of the mitochondrial enzyme acetyl-CoA synthetase 2
journal, June 2006

  • Schwer, B.; Bunkenborg, J.; Verdin, R. O.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 27
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Dedicated ent-kaurene and ent-atiserene synthases for platensimycin and platencin biosynthesis
journal, August 2011

  • Smanski, M. J.; Yu, Z.; Casper, J.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 33
  • DOI: 10.1073/pnas.1106919108

MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods
journal, May 2011

  • Tamura, K.; Peterson, D.; Peterson, N.
  • Molecular Biology and Evolution, Vol. 28, Issue 10
  • DOI: 10.1093/molbev/msr121

Sir2-Dependent Activation of Acetyl-CoA Synthetase by Deacetylation of Active Lysine
journal, December 2002

Amino Acid Biosynthesis and its Regulation
journal, June 1978

Aminoacyl-tRNA Synthesis
journal, June 2000

PHENIX: a comprehensive Python-based system for macromolecular structure solution.
text, January 2010

  • Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
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Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard.
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