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Biosynthesis of GMGT lipids by a radical SAM enzyme associated with anaerobic archaea and oxygen-deficient environments

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  • Yanan Li

    (Southern University of Science and Technology
    Southern University of Science and Technology)

  • Ting Yu

    (Southern University of Science and Technology)

  • Xi Feng

    (Southern University of Science and Technology)

  • Bo Zhao

    (Southern University of Science and Technology)

  • Huahui Chen

    (Southern University of Science and Technology)

  • Huan Yang

    (China University of Geosciences)

  • Xing Chen

    (Ocean University of China)

  • Xiao-Hua Zhang

    (Ocean University of China)

  • Hayden R. Anderson

    (Stanford University)

  • Noah Z. Burns

    (Stanford University)

  • Fuxing Zeng

    (Southern University of Science and Technology)

  • Lizhi Tao

    (Southern University of Science and Technology)

  • Zhirui Zeng

    (Southern University of Science and Technology)

Abstract

Archaea possess characteristic membrane-spanning lipids that are thought to contribute to the adaptation to extreme environments. However, the biosynthesis of these lipids is poorly understood. Here, we identify a radical S-adenosyl-L-methionine (SAM) enzyme that synthesizes glycerol monoalkyl glycerol tetraethers (GMGTs). The enzyme, which we name GMGT synthase (Gms), catalyzes the formation of a C(sp3)–C(sp3) linkage between the two isoprenoid chains of glycerol dialkyl glycerol tetraethers (GDGTs). This conclusion is supported by heterologous expression of gene gms from a GMGT-producing species in a methanogen, as well as demonstration of in vitro activity using purified Gms enzyme. Additionally, we show that genes encoding putative Gms homologs are present in obligate anaerobic archaea and in metagenomes obtained from oxygen-deficient environments, and appear to be absent in metagenomes from oxic settings.

Suggested Citation

  • Yanan Li & Ting Yu & Xi Feng & Bo Zhao & Huahui Chen & Huan Yang & Xing Chen & Xiao-Hua Zhang & Hayden R. Anderson & Noah Z. Burns & Fuxing Zeng & Lizhi Tao & Zhirui Zeng, 2024. "Biosynthesis of GMGT lipids by a radical SAM enzyme associated with anaerobic archaea and oxygen-deficient environments," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49650-x
    DOI: 10.1038/s41467-024-49650-x
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    References listed on IDEAS

    as
    1. Cody T. Lloyd & David F. Iwig & Bo Wang & Matteo Cossu & William W. Metcalf & Amie K. Boal & Squire J. Booker, 2022. "Discovery, structure and mechanism of a tetraether lipid synthase," Nature, Nature, vol. 609(7925), pages 197-203, September.
    2. Steffen Buessecker & Marike Palmer & Dengxun Lai & Joshua Dimapilis & Xavier Mayali & Damon Mosier & Jian-Yu Jiao & Daniel R. Colman & Lisa M. Keller & Emily St. John & Michelle Miranda & Cristina Gon, 2022. "An essential role for tungsten in the ecology and evolution of a previously uncultivated lineage of anaerobic, thermophilic Archaea," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. Zhirui Zeng & Huahui Chen & Huan Yang & Yufei Chen & Wei Yang & Xi Feng & Hongye Pei & Paula V. Welander, 2022. "Identification of a protein responsible for the synthesis of archaeal membrane-spanning GDGT lipids," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    4. Thiago Rodrigues-Oliveira & Florian Wollweber & Rafael I. Ponce-Toledo & Jingwei Xu & Simon K.-M. R. Rittmann & Andreas Klingl & Martin Pilhofer & Christa Schleper, 2023. "Actin cytoskeleton and complex cell architecture in an Asgard archaeon," Nature, Nature, vol. 613(7943), pages 332-339, January.
    5. Laura Eme & Daniel Tamarit & Eva F. Caceres & Courtney W. Stairs & Valerie Anda & Max E. Schön & Kiley W. Seitz & Nina Dombrowski & William H. Lewis & Felix Homa & Jimmy H. Saw & Jonathan Lombard & Ta, 2023. "Inference and reconstruction of the heimdallarchaeial ancestry of eukaryotes," Nature, Nature, vol. 618(7967), pages 992-999, June.
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