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Expression of Vibrio harveyi Acyl-ACP Synthetase Allows Efficient Entry of Exogenous Fatty Acids into the Escherichia coli Fatty Acid and Lipid A Synthetic Pathways

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    Article

    Expression of Vibrio harveyi Acyl-ACP Synthetase Allows Efficient Entry of Exogenous Fatty Acids into the Escherichia coli Fatty Acid and Lipid A Synthetic Pathways
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    ‡ Department of Microbiology
    § Department of Biochemistry
    University of Illinois, Urbana, Illinois 61801.
    *To whom correspondence should be addressed. Phone: (217) 333-7919. Fax: (217) 244-6697. E-mail: [email protected]
    ∥Present address: Department of Molecular Microbiology, Washington University School of Medicine, 660 S. Euclid Ave., St. Louis, MO 63110-1093.
    ⊥Present address: Department of Microbiology, Miami University, Oxford, OH 45056.
    @Present address: Scarab Genomics, LLC, 1202 Ann St., Madison, WI 53713.
    #Present address: Department of Bacteriology, Room 1322, Microbial Sciences Building, 1550 Linden Dr., Madison, WI 53706.
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    Biochemistry

    Cite this: Biochemistry 2010, 49, 4, 718–726
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    https://doi.org/10.1021/bi901890a
    Published December 22, 2009
    Copyright © 2009 American Chemical Society
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    Abstract

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    Although the Escherichia coli fatty acid synthesis (FAS) pathway is the best studied type II fatty acid synthesis system, a major experimental limitation has been the inability to feed intermediates into the pathway in vivo because exogenously supplied free fatty acids are not efficiently converted to the acyl−acyl carrier protein (ACP) thioesters required by the pathway. We report that expression of Vibrio harveyi acyl-ACP synthetase (AasS), a soluble cytosolic enzyme that ligates free fatty acids to ACP to form acyl-ACPs, allows exogenous fatty acids to enter the E. coli fatty acid synthesis pathway. The free fatty acids are incorporated intact and can be elongated or directly incorporated into complex lipids by acyltransferases specific for acyl-ACPs. Moreover, expression of AasS strains and supplementation with the appropriate fatty acid restored growth to E. coli mutant strains that lack essential fatty acid synthesis enzymes. Thus, this strategy provides a new tool for circumventing the loss of enzymes essential for FAS function.

    Copyright © 2009 American Chemical Society

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    Analyses of the genetic constructs, mass spectra, a table of mass spectroscopic values, and figures of data characterizing the endogenous elongation activity. This material is available free of charge via the Internet at http://pubs.acs.org.

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    Cited By

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    This article is cited by 38 publications.

    1. Janine G. Borgaro, Andrew Chang, Carl A. Machutta, Xujie Zhang, and Peter J. Tonge . Substrate Recognition by β-Ketoacyl-ACP Synthases. Biochemistry 2011, 50 (49) , 10678-10686. https://doi.org/10.1021/bi201199x
    2. Lucas M. Demey, Ritam Sinha, Victor J. DiRita, . An essential host dietary fatty acid promotes TcpH inhibition of TcpP proteolysis promoting virulence gene expression in Vibrio cholerae. mBio 2024, 15 (8) https://doi.org/10.1128/mbio.00721-24
    3. Haomin Huang, Shenghai Chang, Tao Cui, Man Huang, Jiuxin Qu, Huimin Zhang, Ting Lu, Xing Zhang, Chun Zhou, Youjun Feng, . An inhibitory mechanism of AasS, an exogenous fatty acid scavenger: Implications for re-sensitization of FAS II antimicrobials. PLOS Pathogens 2024, 20 (7) , e1012376. https://doi.org/10.1371/journal.ppat.1012376
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    5. John E. Cronan. The acyl carrier proteins of lipid synthesis are busy having other affairs. Biochemical Journal 2023, 480 (12) , 855-873. https://doi.org/10.1042/BCJ20230161
    6. Huijuan Dong, John E. Cronan. Unsaturated fatty acid synthesis in Enterococcus faecalis requires a specific enoyl‐ACP reductase. Molecular Microbiology 2022, 118 (5) , 541-551. https://doi.org/10.1111/mmi.14981
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    8. Yongchang Xu, Jie Yang, Weihui Li, Shuaijie Song, Yu Shi, Lihan Wu, Jingdu Sun, Mengyun Hou, Jinzi Wang, Xu Jia, Huimin Zhang, Man Huang, Ting Lu, Jianhua Gan, Youjun Feng, . Three enigmatic BioH isoenzymes are programmed in the early stage of mycobacterial biotin synthesis, an attractive anti-TB drug target. PLOS Pathogens 2022, 18 (7) , e1010615. https://doi.org/10.1371/journal.ppat.1010615
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    10. Sandra A. C. Figueiredo, Marco Preto, Gabriela Moreira, Teresa P. Martins, Kathleen Abt, André Melo, Vitor M. Vasconcelos, Pedro N. Leão. Discovery of Cyanobacterial Natural Products Containing Fatty Acid Residues**. Angewandte Chemie 2021, 133 (18) , 10152-10160. https://doi.org/10.1002/ange.202015105
    11. Sandra A. C. Figueiredo, Marco Preto, Gabriela Moreira, Teresa P. Martins, Kathleen Abt, André Melo, Vitor M. Vasconcelos, Pedro N. Leão. Discovery of Cyanobacterial Natural Products Containing Fatty Acid Residues**. Angewandte Chemie International Edition 2021, 60 (18) , 10064-10072. https://doi.org/10.1002/anie.202015105
    12. Yuanyuan Hu, John E. Cronan. α-proteobacteria synthesize biotin precursor pimeloyl-ACP using BioZ 3-ketoacyl-ACP synthase and lysine catabolism. Nature Communications 2020, 11 (1) https://doi.org/10.1038/s41467-020-19251-5
    13. Christopher D. Radka, Matthew W. Frank, Charles O. Rock, Jiangwei Yao. Fatty acid activation and utilization by Alistipes finegoldii , a representative Bacteroidetes resident of the human gut microbiome. Molecular Microbiology 2020, 113 (4) , 807-825. https://doi.org/10.1111/mmi.14445
    14. Jianjiang Ma, Ji Liu, Wenfeng Pei, Qifeng Ma, Nuohan Wang, Xia Zhang, Yupeng Cui, Dan Li, Guoyuan Liu, Man Wu, XinShan Zang, Jikun Song, Jinfa Zhang, Shuxun Yu, Jiwen Yu. Genome-wide association study of the oil content in upland cotton (Gossypium hirsutum L.) and identification of GhPRXR1, a candidate gene for a stable QTLqOC-Dt5-1. Plant Science 2019, 286 , 89-97. https://doi.org/10.1016/j.plantsci.2019.05.019
    15. Jiangwei Yao, Charles O. Rock. Therapeutic Targets in Chlamydial Fatty Acid and Phospholipid Synthesis. Frontiers in Microbiology 2018, 9 https://doi.org/10.3389/fmicb.2018.02291
    16. Yanbin Feng, Yunxiu Zhang, Yayue Wang, Jiao Liu, Yinghui Liu, Xupeng Cao, Song Xue. Tuning of acyl-ACP thioesterase activity directed for tailored fatty acid synthesis. Applied Microbiology and Biotechnology 2018, 102 (7) , 3173-3182. https://doi.org/10.1007/s00253-018-8770-6
    17. Jiangwei Yao, Charles O. Rock. Exogenous fatty acid metabolism in bacteria. Biochimie 2017, 141 , 30-39. https://doi.org/10.1016/j.biochi.2017.06.015
    18. Hongkai Bi, Lei Zhu, Jia Jia, Liping Zeng, John E. Cronan. Unsaturated Fatty Acid Synthesis in the Gastric Pathogen Helicobacter pylori Proceeds via a Backtracking Mechanism. Cell Chemical Biology 2016, 23 (12) , 1480-1489. https://doi.org/10.1016/j.chembiol.2016.10.007
    19. Gayle J. Bentley, Wen Jiang, Linda P. Guamán, Yi Xiao, Fuzhong Zhang. Engineering Escherichia coli to produce branched-chain fatty acids in high percentages. Metabolic Engineering 2016, 38 , 148-158. https://doi.org/10.1016/j.ymben.2016.07.003
    20. Joris Beld, Raffaela Abbriano, Kara Finzel, Mark Hildebrand, Michael D. Burkart. Probing fatty acid metabolism in bacteria, cyanobacteria, green microalgae and diatoms with natural and unnatural fatty acids. Molecular BioSystems 2016, 12 (4) , 1299-1312. https://doi.org/10.1039/C5MB00804B
    21. Jiangwei Yao, David F. Bruhn, Matthew W. Frank, Richard E. Lee, Charles O. Rock. Activation of Exogenous Fatty Acids to Acyl-Acyl Carrier Protein Cannot Bypass FabI Inhibition in Neisseria. Journal of Biological Chemistry 2016, 291 (1) , 171-181. https://doi.org/10.1074/jbc.M115.699462
    22. Jiangwei Yao, Charles O. Rock. How Bacterial Pathogens Eat Host Lipids: Implications for the Development of Fatty Acid Synthesis Therapeutics. Journal of Biological Chemistry 2015, 290 (10) , 5940-5946. https://doi.org/10.1074/jbc.R114.636241
    23. Joshua B. Parsons, Jiangwei Yao, Matthew W. Frank, Charles O. Rock. FabH Mutations Confer Resistance to FabF-Directed Antibiotics in Staphylococcus aureus. Antimicrobial Agents and Chemotherapy 2015, 59 (2) , 849-858. https://doi.org/10.1128/AAC.04179-14
    24. Joris Beld, D. John Lee, Michael D. Burkart. Fatty acid biosynthesis revisited: structure elucidation and metabolic engineering. Molecular BioSystems 2015, 11 (1) , 38-59. https://doi.org/10.1039/C4MB00443D
    25. P. Peters-Wendisch, S. Götker, S.A.E. Heider, G. Komati Reddy, A.Q. Nguyen, K.C. Stansen, V.F. Wendisch. Engineering biotin prototrophic Corynebacterium glutamicum strains for amino acid, diamine and carotenoid production. Journal of Biotechnology 2014, 192 , 346-354. https://doi.org/10.1016/j.jbiotec.2014.01.023
    26. Joris Beld, Kara Finzel, Michael D. Burkart. Versatility of Acyl-Acyl Carrier Protein Synthetases. Chemistry & Biology 2014, 21 (10) , 1293-1299. https://doi.org/10.1016/j.chembiol.2014.08.015
    27. Hongkai Bi, Yonghong Yu, Huijuan Dong, Haihong Wang, John E. Cronan. X anthomonas campestris  RpfB is a fatty Acyl-CoA ligase required to counteract the thioesterase activity of the RpfF diffusible signal factor (DSF) synthase. Molecular Microbiology 2014, 93 (2) , 262-275. https://doi.org/10.1111/mmi.12657
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    31. Hongkai Bi, Haihong Wang, John E. Cronan. FabQ, a Dual-Function Dehydratase/Isomerase, Circumvents the Last Step of the Classical Fatty Acid Synthesis Cycle. Chemistry & Biology 2013, 20 (9) , 1157-1167. https://doi.org/10.1016/j.chembiol.2013.07.007
    32. Catherine Tardy-Laporte, Alexandre A. Arnold, Bertrand Genard, Romain Gastineau, Michèle Morançais, Jean-Luc Mouget, Réjean Tremblay, Isabelle Marcotte. A 2H solid-state NMR study of the effect of antimicrobial agents on intact Escherichia coli without mutating. Biochimica et Biophysica Acta (BBA) - Biomembranes 2013, 1828 (2) , 614-622. https://doi.org/10.1016/j.bbamem.2012.09.011
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    Biochemistry

    Cite this: Biochemistry 2010, 49, 4, 718–726
    Click to copy citationCitation copied!
    https://doi.org/10.1021/bi901890a
    Published December 22, 2009
    Copyright © 2009 American Chemical Society
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