Rao, Bhagyashree Dasari and Gomez-Gil, Elisa and Péter, Mária and Balogh, Gábor and Nunes, Vanessa and MacRae, James I. and Chen, Qu and Rosenthal, Peter B. and Oliferenko, Snezhana (2025) Horizontal acquisition of prokaryotic hopanoid biosynthesis reorganizes membrane physiology driving lifestyle innovation in a eukaryote. NATURE COMMUNICATIONS, 16 (1). No. 3291. ISSN 2041-1723
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Abstract
Horizontal gene transfer is a source of metabolic innovation and adaptation to new environments. How new metabolic functionalities are integrated into host cell biology is largely unknown. Here, we probe this fundamental question using the fission yeast Schizosaccharomyces japonicus, which has acquired a squalene-hopene cyclase Shc1 through horizontal gene transfer. We show that Shc1-dependent production of hopanoids, mimics of eukaryotic sterols, allows S. japonicus to thrive in anoxia, where sterol biosynthesis is not possible. We demonstrate that glycerophospholipid fatty acyl asymmetry, prevalent in S. japonicus, is crucial for accommodating both sterols and hopanoids in membranes and explain how Shc1 functions alongside the sterol biosynthetic pathway to support membrane properties. Reengineering experiments in the sister species S. pombe show that hopanoids entail new traits in a na & iuml;ve organism, but the acquisition of a new enzyme may trigger profound reorganization of the host metabolism and physiology.
| Item Type: | Article |
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| Additional Information: | Funding Agency and Grant Number: EMBO postdoctoral fellowship; UKRI guarantee of a MSCA postdoctoral fellowship; EU [KIM NKFIA 2022-2.1.1-NL-2022-00005]; Francis Crick Institute [CC2106]; Cancer Research UK [CC0102]; UK Medical Research Council; Wellcome Trust [103741/Z/14/Z, 220790/Z/20/Z]; [ALTF 712-2022]; [EP/Y024702/1]; [739593]; Wellcome Trust [220790/Z/20/Z] Funding Source: Wellcome Trust Funding text: We are grateful to the Oliferenko lab for discussions and Eugene Makeyev for suggestions on the manuscript. Many thanks to Fred Betts Thompson for media preparations, Nikita Komarov for helping with shc1 Delta mutant construction, Laura Masino for advice on spectroscopy, and to the Crick Metabolomics, Light Microscopy and Structural Biology STPs for invaluable training and assistance. We thank Dylan Herzog, Vincenzo Infante and Stefania Marcotti at the King's Nikon Imaging Centre for their help in setting up live cell membrane order measurements. Elisa Gomez-Gil has been supported through a long-term EMBO postdoctoral fellowship (ALTF 712-2022, E.G.G.) and the UKRI guarantee of a MSCA postdoctoral fellowship (EP/Y024702/1, E.G.G). We thank the Single Cell Omics Advanced Core Facility staff of the HCEMM and Biological Research Center for help with their resources and their support. HCEMM has received funding from the EU's Horizon 2020 research and innovation program under grant agreement No. 739593 and KIM NKFIA 2022-2.1.1-NL-2022-00005. The work in the Rosenthal lab is supported through grant CC2106 from the Francis Crick Institute. This work was supported by the Francis Crick Institute, which receives its core funding from Cancer Research UK (CC0102), the UK Medical Research Council (CC0102), and the Wellcome Trust (CC0102), and the Wellcome Trust Senior Investigator Award (103741/Z/14/Z) and Wellcome Trust Investigator Award in Science (220790/Z/20/Z) to S.O. |
| Uncontrolled Keywords: | DOMAINS; organization; integration; EFFICIENT; cholesterol; FISSION YEAST; Laurdan; fluorescence probe; squalene epoxidase; |
| Subjects: | Q Science / természettudomány > QH Natural history / természetrajz > QH301 Biology / biológia |
| SWORD Depositor: | MTMT SWORD |
| Depositing User: | MTMT SWORD |
| Date Deposited: | 17 Mar 2026 15:42 |
| Last Modified: | 17 Mar 2026 15:42 |
| URI: | https://real.mtak.hu/id/eprint/235775 |
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