IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-54259-1.html
   My bibliography  Save this article

Tuning architectural organization of eukaryotic P450 system to boost bioproduction in Escherichia coli

Author

Listed:
  • Yikui Li

    (Jiangsu Province and Chinese Academy of Sciences
    Jiangsu Key Laboratory for the Research and Utilization of Plant Resources
    Nanjing Botanical Garden Mem. Sun Yat-Sen)

  • Jie Li

    (Jiangsu Province and Chinese Academy of Sciences
    Jiangsu Key Laboratory for the Research and Utilization of Plant Resources
    Nanjing Botanical Garden Mem. Sun Yat-Sen)

  • Wei-Kang Chen

    (Jiangsu Province and Chinese Academy of Sciences)

  • Yang Li

    (Jiangsu Province and Chinese Academy of Sciences)

  • Sheng Xu

    (Jiangsu Province and Chinese Academy of Sciences
    Jiangsu Key Laboratory for the Research and Utilization of Plant Resources
    Nanjing Botanical Garden Mem. Sun Yat-Sen)

  • Linwei Li

    (Jiangsu Province and Chinese Academy of Sciences)

  • Bing Xia

    (Jiangsu Province and Chinese Academy of Sciences
    Jiangsu Key Laboratory for the Research and Utilization of Plant Resources
    Nanjing Botanical Garden Mem. Sun Yat-Sen)

  • Ren Wang

    (Jiangsu Province and Chinese Academy of Sciences
    Jiangsu Key Laboratory for the Research and Utilization of Plant Resources
    Nanjing Botanical Garden Mem. Sun Yat-Sen)

Abstract

Eukaryotic cytochrome P450 enzymes, generally colocalizing with their redox partner cytochrome P450 reductase (CPR) on the cytoplasmic surface of organelle membranes, often perform poorly in prokaryotic cells, whether expressed with CPR as a tandem chimera or free-floating individuals, causing a low titer of heterologous chemicals. To improve their biosynthetic performance in Escherichia coli, here, we architecturally design self-assembled alternatives of eukaryotic P450 system using reconstructed P450 and CPR, and create a set of N-termini-bridged P450-CPR heterodimers as the counterparts of eukaryotic P450 system with N-terminus-guided colocalization. The covalent counterparts show superior and robust biosynthetic performance, and the N-termini-bridged architecture is validated to improve the biosynthetic performance of both plant and human P450 systems. Furthermore, the architectural configuration of protein assemblies has an inherent effect on the biosynthetic performance of N-termini-bridged P450-CPR heterodimers. The results suggest that spatial architecture-guided protein assembly could serve as an efficient strategy for improving the biosynthetic performance of protein complexes, particularly those related to eukaryotic membranes, in prokaryotic and even eukaryotic hosts.

Suggested Citation

  • Yikui Li & Jie Li & Wei-Kang Chen & Yang Li & Sheng Xu & Linwei Li & Bing Xia & Ren Wang, 2024. "Tuning architectural organization of eukaryotic P450 system to boost bioproduction in Escherichia coli," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-54259-1
    DOI: 10.1038/s41467-024-54259-1
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-54259-1
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-54259-1?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. C. J. Paddon & P. J. Westfall & D. J. Pitera & K. Benjamin & K. Fisher & D. McPhee & M. D. Leavell & A. Tai & A. Main & D. Eng & D. R. Polichuk & K. H. Teoh & D. W. Reed & T. Treynor & J. Lenihan & H., 2013. "High-level semi-synthetic production of the potent antimalarial artemisinin," Nature, Nature, vol. 496(7446), pages 528-532, April.
    2. Lee J. Sweetlove & Alisdair R. Fernie, 2018. "The role of dynamic enzyme assemblies and substrate channelling in metabolic regulation," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    3. Ruijie K. Zhang & Kai Chen & Xiongyi Huang & Lena Wohlschlager & Hans Renata & Frances H. Arnold, 2019. "Enzymatic assembly of carbon–carbon bonds via iron-catalysed sp3 C–H functionalization," Nature, Nature, vol. 565(7737), pages 67-72, January.
    4. Jing-Dong J. Han & Nicolas Bertin & Tong Hao & Debra S. Goldberg & Gabriel F. Berriz & Lan V. Zhang & Denis Dupuy & Albertha J. M. Walhout & Michael E. Cusick & Frederick P. Roth & Marc Vidal, 2004. "Erratum: Evidence for dynamically organized modularity in the yeast protein–protein interaction network," Nature, Nature, vol. 430(6997), pages 380-380, July.
    5. Jing-Dong J. Han & Nicolas Bertin & Tong Hao & Debra S. Goldberg & Gabriel F. Berriz & Lan V. Zhang & Denis Dupuy & Albertha J. M. Walhout & Michael E. Cusick & Frederick P. Roth & Marc Vidal, 2004. "Evidence for dynamically organized modularity in the yeast protein–protein interaction network," Nature, Nature, vol. 430(6995), pages 88-93, July.
    6. Dae-Kyun Ro & Eric M. Paradise & Mario Ouellet & Karl J. Fisher & Karyn L. Newman & John M. Ndungu & Kimberly A. Ho & Rachel A. Eachus & Timothy S. Ham & James Kirby & Michelle C. Y. Chang & Sydnor T., 2006. "Production of the antimalarial drug precursor artemisinic acid in engineered yeast," Nature, Nature, vol. 440(7086), pages 940-943, April.
    7. Jorge Roel-Touris & Brian Jiménez-García & Alexandre M. J. J. Bonvin, 2020. "Integrative modeling of membrane-associated protein assemblies," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    8. Xiaozhou Luo & Michael A. Reiter & Leo d’Espaux & Jeff Wong & Charles M. Denby & Anna Lechner & Yunfeng Zhang & Adrian T. Grzybowski & Simon Harth & Weiyin Lin & Hyunsu Lee & Changhua Yu & John Shin &, 2019. "Complete biosynthesis of cannabinoids and their unnatural analogues in yeast," Nature, Nature, vol. 567(7746), pages 123-126, March.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Jack Chun-Ting Liu & Ricardo De La Peña & Christian Tocol & Elizabeth S. Sattely, 2024. "Reconstitution of early paclitaxel biosynthetic network," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    2. Pan-Jun Kim & Nathan D Price, 2011. "Genetic Co-Occurrence Network across Sequenced Microbes," PLOS Computational Biology, Public Library of Science, vol. 7(12), pages 1-9, December.
    3. Ashty S. Karim & Dylan M. Brown & Chloé M. Archuleta & Sharisse Grannan & Ludmilla Aristilde & Yogesh Goyal & Josh N. Leonard & Niall M. Mangan & Arthur Prindle & Gabriel J. Rocklin & Keith J. Tyo & L, 2024. "Deconstructing synthetic biology across scales: a conceptual approach for training synthetic biologists," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    4. Seyed Yahya Anvar & Allan Tucker & Veronica Vinciotti & Andrea Venema & Gert-Jan B van Ommen & Silvere M van der Maarel & Vered Raz & Peter A C ‘t Hoen, 2011. "Interspecies Translation of Disease Networks Increases Robustness and Predictive Accuracy," PLOS Computational Biology, Public Library of Science, vol. 7(11), pages 1-14, November.
    5. Peter Langfelder & Paul S Mischel & Steve Horvath, 2013. "When Is Hub Gene Selection Better than Standard Meta-Analysis?," PLOS ONE, Public Library of Science, vol. 8(4), pages 1-16, April.
    6. Fabio Cumbo & Paola Paci & Daniele Santoni & Luisa Di Paola & Alessandro Giuliani, 2014. "GIANT: A Cytoscape Plugin for Modular Networks," PLOS ONE, Public Library of Science, vol. 9(10), pages 1-7, October.
    7. Weijiang Li & Hiroyuki Kurata, 2008. "Visualizing Global Properties of Large Complex Networks," PLOS ONE, Public Library of Science, vol. 3(7), pages 1-4, July.
    8. Yau-Hua Yu & Hsu-Ko Kuo & Kuo-Wei Chang, 2008. "The Evolving Transcriptome of Head and Neck Squamous Cell Carcinoma: A Systematic Review," PLOS ONE, Public Library of Science, vol. 3(9), pages 1-11, September.
    9. Chrysafis Vogiatzis & Mustafa Can Camur, 2019. "Identification of Essential Proteins Using Induced Stars in Protein–Protein Interaction Networks," INFORMS Journal on Computing, INFORMS, vol. 31(4), pages 703-718, October.
    10. Gabor I Simko & Peter Csermely, 2013. "Nodes Having a Major Influence to Break Cooperation Define a Novel Centrality Measure: Game Centrality," PLOS ONE, Public Library of Science, vol. 8(6), pages 1-8, June.
    11. Shiwei Lu & Yaping Huang & Zhiyuan Zhao & Xiping Yang, 2018. "Exploring the Hierarchical Structure of China’s Railway Network from 2008 to 2017," Sustainability, MDPI, vol. 10(9), pages 1-15, September.
    12. Franke, R., 2016. "CHIMERA: Top-down model for hierarchical, overlapping and directed cluster structures in directed and weighted complex networks," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 461(C), pages 384-408.
    13. Anna Zimmermann & Julian E. Prieto-Vivas & Charlotte Cautereels & Anton Gorkovskiy & Jan Steensels & Yves Peer & Kevin J. Verstrepen, 2023. "A Cas3-base editing tool for targetable in vivo mutagenesis," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    14. Patrick C F Buchholz & Catharina Zeil & Jürgen Pleiss, 2018. "The scale-free nature of protein sequence space," PLOS ONE, Public Library of Science, vol. 13(8), pages 1-14, August.
    15. Hou, Bonan & Yao, Yiping & Liao, Dongsheng, 2012. "Identifying all-around nodes for spreading dynamics in complex networks," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 391(15), pages 4012-4017.
    16. Zhang, Yuerong & Marshall, Stephen & Manley, Ed, 2021. "Understanding the roles of rail stations: Insights from network approaches in the London metropolitan area," Journal of Transport Geography, Elsevier, vol. 94(C).
    17. Changki Hong & Jeewon Hwang & Kwang-Hyun Cho & Insik Shin, 2015. "An Efficient Steady-State Analysis Method for Large Boolean Networks with High Maximum Node Connectivity," PLOS ONE, Public Library of Science, vol. 10(12), pages 1-19, December.
    18. Seah Choon Sen & Shahreen Kasim & Mohd Farhan Md Fudzee & Rusli Abdullah & Rodziah Atan, 2017. "Random Walk From Different Perspective," Acta Electronica Malaysia (AEM), Zibeline International Publishing, vol. 1(2), pages 26-27, November.
    19. Luis P Fernandes & Alessia Annibale & Jens Kleinjung & Anthony C C Coolen & Franca Fraternali, 2010. "Protein Networks Reveal Detection Bias and Species Consistency When Analysed by Information-Theoretic Methods," PLOS ONE, Public Library of Science, vol. 5(8), pages 1-14, August.
    20. Sun, Yeran & Mburu, Lucy & Wang, Shaohua, 2016. "Analysis of community properties and node properties to understand the structure of the bus transport network," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 450(C), pages 523-530.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-54259-1. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.