IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-40242-9.html
   My bibliography  Save this article

A tripartite microbial co-culture system for de novo biosynthesis of diverse plant phenylpropanoids

Author

Listed:
  • Sierra M. Brooks

    (The University of Texas at Austin)

  • Celeste Marsan

    (The University of Texas at Austin)

  • Kevin B. Reed

    (The University of Texas at Austin)

  • Shuo-Fu Yuan

    (The University of Texas at Austin)

  • Dustin-Dat Nguyen

    (The University of Texas at Austin)

  • Adit Trivedi

    (The University of Texas at Austin)

  • Gokce Altin-Yavuzarslan

    (University of Washington)

  • Nathan Ballinger

    (University of Washington)

  • Alshakim Nelson

    (University of Washington
    University of Washington)

  • Hal S. Alper

    (The University of Texas at Austin
    The University of Texas at Austin)

Abstract

Plant-derived phenylpropanoids, in particular phenylpropenes, have diverse industrial applications ranging from flavors and fragrances to polymers and pharmaceuticals. Heterologous biosynthesis of these products has the potential to address low, seasonally dependent yields hindering ease of widespread manufacturing. However, previous efforts have been hindered by the inherent pathway promiscuity and the microbial toxicity of key pathway intermediates. Here, in this study, we establish the propensity of a tripartite microbial co-culture to overcome these limitations and demonstrate to our knowledge the first reported de novo phenylpropene production from simple sugar starting materials. After initially designing the system to accumulate eugenol, the platform modularity and downstream enzyme promiscuity was leveraged to quickly create avenues for hydroxychavicol and chavicol production. The consortia was found to be compatible with Engineered Living Material production platforms that allow for reusable, cold-chain-independent distributed manufacturing. This work lays the foundation for further deployment of modular microbial approaches to produce plant secondary metabolites.

Suggested Citation

  • Sierra M. Brooks & Celeste Marsan & Kevin B. Reed & Shuo-Fu Yuan & Dustin-Dat Nguyen & Adit Trivedi & Gokce Altin-Yavuzarslan & Nathan Ballinger & Alshakim Nelson & Hal S. Alper, 2023. "A tripartite microbial co-culture system for de novo biosynthesis of diverse plant phenylpropanoids," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40242-9
    DOI: 10.1038/s41467-023-40242-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-40242-9
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-40242-9?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. Prashanth Srinivasan & Christina D. Smolke, 2020. "Biosynthesis of medicinal tropane alkaloids in yeast," Nature, Nature, vol. 585(7826), pages 614-619, September.
    2. Trevor G. Johnston & Shuo-Fu Yuan & James M. Wagner & Xiunan Yi & Abhijit Saha & Patrick Smith & Alshakim Nelson & Hal S. Alper, 2020. "Compartmentalized microbes and co-cultures in hydrogels for on-demand bioproduction and preservation," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    3. Jie Zhang & Lea G. Hansen & Olga Gudich & Konrad Viehrig & Lærke M. M. Lassen & Lars Schrübbers & Khem B. Adhikari & Paulina Rubaszka & Elena Carrasquer-Alvarez & Ling Chen & Vasil D’Ambrosio & Beata , 2022. "A microbial supply chain for production of the anti-cancer drug vinblastine," Nature, Nature, vol. 609(7926), pages 341-347, September.
    4. Sierra M. Brooks & Hal S. Alper, 2021. "Applications, challenges, and needs for employing synthetic biology beyond the lab," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    5. Xiaonan Liu & Jian Cheng & Guanghui Zhang & Wentao Ding & Lijin Duan & Jing Yang & Ling Kui & Xiaozhi Cheng & Jiangxing Ruan & Wei Fan & Junwen Chen & Guangqiang Long & Yan Zhao & Jing Cai & Wen Wang , 2018. "Engineering yeast for the production of breviscapine by genomic analysis and synthetic biology approaches," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    6. Wenna Li & Zhao Zhou & Xianglai Li & Lin Ma & Qingyuan Guan & Guojun Zheng & Hao Liang & Yajun Yan & Xiaolin Shen & Jia Wang & Xinxiao Sun & Qipeng Yuan, 2022. "Biosynthesis of plant hemostatic dencichine in Escherichia coli," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    7. 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. Wenna Li & Zhao Zhou & Xianglai Li & Lin Ma & Qingyuan Guan & Guojun Zheng & Hao Liang & Yajun Yan & Xiaolin Shen & Jia Wang & Xinxiao Sun & Qipeng Yuan, 2022. "Biosynthesis of plant hemostatic dencichine in Escherichia coli," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    2. Xiang Jiao & Xiaozhi Fu & Qishuang Li & Junling Bu & Xiuyu Liu & Otto Savolainen & Luqi Huang & Juan Guo & Jens Nielsen & Yun Chen, 2024. "De novo production of protoberberine and benzophenanthridine alkaloids through metabolic engineering of yeast," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    3. Gita Naseri, 2023. "A roadmap to establish a comprehensive platform for sustainable manufacturing of natural products in yeast," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    4. 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.
    5. Ruiqi Yan & Binghan Xie & Kebo Xie & Qi Liu & Songyang Sui & Shuqi Wang & Dawei Chen & Jimei Liu & Ridao Chen & Jungui Dai & Lin Yang, 2024. "Unravelling and reconstructing the biosynthetic pathway of bergenin," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    6. Yue Gao & Fei Li & Zhengshan Luo & Zhiwei Deng & Yan Zhang & Zhenbo Yuan & Changmei Liu & Yijian Rao, 2024. "Modular assembly of an artificially concise biocatalytic cascade for the manufacture of phenethylisoquinoline alkaloids," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    7. Simon d’Oelsnitz & Daniel J. Diaz & Wantae Kim & Daniel J. Acosta & Tyler L. Dangerfield & Mason W. Schechter & Matthew B. Minus & James R. Howard & Hannah Do & James M. Loy & Hal S. Alper & Y. Jessie, 2024. "Biosensor and machine learning-aided engineering of an amaryllidaceae enzyme," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    8. Christopher J. Vavricka & Shunsuke Takahashi & Naoki Watanabe & Musashi Takenaka & Mami Matsuda & Takanobu Yoshida & Ryo Suzuki & Hiromasa Kiyota & Jianyong Li & Hiromichi Minami & Jun Ishii & Kenji T, 2022. "Machine learning discovery of missing links that mediate alternative branches to plant alkaloids," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    9. Qun Yue & Jie Meng & Yue Qiu & Miaomiao Yin & Liwen Zhang & Weiping Zhou & Zhiqiang An & Zihe Liu & Qipeng Yuan & Wentao Sun & Chun Li & Huimin Zhao & István Molnár & Yuquan Xu & Shuobo Shi, 2023. "A polycistronic system for multiplexed and precalibrated expression of multigene pathways in fungi," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    10. Yuanwei Gou & Dongfang Li & Minghui Zhao & Mengxin Li & Jiaojiao Zhang & Yilian Zhou & Feng Xiao & Gaofei Liu & Haote Ding & Chenfan Sun & Cuifang Ye & Chang Dong & Jucan Gao & Di Gao & Zehua Bao & Le, 2024. "Intein-mediated temperature control for complete biosynthesis of sanguinarine and its halogenated derivatives in yeast," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    11. Li Tang & Jennifer Kuzma & Xi Zhang & Xinyu Song & Yin Li & Hongxu Liu & Guangyuan Hu, 2023. "Synthetic biology and governance research in China: a 40-year evolution," Scientometrics, Springer;Akadémiai Kiadó, vol. 128(9), pages 5293-5310, September.
    12. William M. Shaw & Yunfeng Zhang & Xinyu Lu & Ahmad S. Khalil & Graham Ladds & Xiaozhou Luo & Tom Ellis, 2022. "Screening microbially produced Δ9-tetrahydrocannabinol using a yeast biosensor workflow," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    13. Shao-Yang Li & Gao-Qian Wang & Liang Long & Jia-Ling Gao & Zheng-Qun Zhou & Yong-Heng Wang & Jian-Ming Lv & Guo-Dong Chen & Dan Hu & Ikuro Abe & Hao Gao, 2024. "Functional and structural dissection of glycosyltransferases underlying the glycodiversity of wolfberry-derived bioactive ingredients lycibarbarspermidines," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    14. 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.
    15. Radin Sadre & Thilani M. Anthony & Josh M. Grabar & Matthew A. Bedewitz & A. Daniel Jones & Cornelius S. Barry, 2022. "Metabolomics-guided discovery of cytochrome P450s involved in pseudotropine-dependent biosynthesis of modified tropane alkaloids," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    16. Yangteng Ou & Shixiang Cao & Yang Zhang & Hongjia Zhu & Chengzhi Guo & Wei Yan & Fengxue Xin & Weiliang Dong & Yanli Zhang & Masashi Narita & Ziyi Yu & Tuomas P. J. Knowles, 2023. "Bioprinting microporous functional living materials from protein-based core-shell microgels," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    17. So-Hee Son & Jae-Eung Kim & Gyuri Park & Young-Joon Ko & Bong Hyun Sung & Jongcheol Seo & Seung Soo Oh & Ju Young Lee, 2022. "Metabolite trafficking enables membrane-impermeable-terpene secretion by yeast," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    18. Jun Guo & Di Gao & Jiazhang Lian & Yang Qu, 2024. "De novo biosynthesis of antiarrhythmic alkaloid ajmaline," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    19. Tian Tian & Yong-Jiang Wang & Jian-Ping Huang & Jie Li & Bingyan Xu & Yin Chen & Li Wang & Jing Yang & Yijun Yan & Sheng-Xiong Huang, 2022. "Catalytic innovation underlies independent recruitment of polyketide synthases in cocaine and hyoscyamine biosynthesis," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    20. Junlan Zeng & Xiaoqiang Liu & Zhaoyue Dong & Fangyuan Zhang & Fei Qiu & Mingyu Zhong & Tengfei Zhao & Chunxian Yang & Lingjiang Zeng & Xiaozhong Lan & Hongbo Zhang & Junhui Zhou & Min Chen & Kexuan Ta, 2024. "Discovering a mitochondrion-localized BAHD acyltransferase involved in calystegine biosynthesis and engineering the production of 3β-tigloyloxytropane," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

    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:14:y:2023:i:1:d:10.1038_s41467-023-40242-9. 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.