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Inositol lipid synthesis is widespread in host-associated Bacteroidetes

S. L. Heaver, H. H. Le, P. Tang, A. Baslé, View ORCID ProfileJ. Marles-Wright, E. L. Johnson, D. J. Campopiano, View ORCID ProfileR. E. Ley
doi: https://doi.org/10.1101/2021.04.26.441525
S. L. Heaver
1Department of Microbiome Science, Max Planck Institute for Developmental Biology, Tübingen 72076, Germany
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H. H. Le
2Division of Nutritional Sciences, Cornell University, Ithaca, NY 14853, USA
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P. Tang
3School of Chemistry, University of Edinburgh, Edinburgh, Scotland, UK
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A. Baslé
4Newcastle University Biosciences Institute, Newcastle University, UK
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J. Marles-Wright
5School of Natural and Environmental Sciences, Newcastle University, UK
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  • ORCID record for J. Marles-Wright
E. L. Johnson
2Division of Nutritional Sciences, Cornell University, Ithaca, NY 14853, USA
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D. J. Campopiano
3School of Chemistry, University of Edinburgh, Edinburgh, Scotland, UK
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R. E. Ley
1Department of Microbiome Science, Max Planck Institute for Developmental Biology, Tübingen 72076, Germany
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  • ORCID record for R. E. Ley
  • For correspondence: rley@tuebingen.mpg.de
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Abstract

Ubiquitous in eukaryotes, inositol lipids have finely tuned roles in cellular signaling and membrane homeostasis. In Bacteria, however, inositol lipid production is rare. Recently, the prominent human gut bacterium Bacteroides thetaiotaomicron (BT) was reported to produce inositol lipids, including inositol sphingolipids, but the pathways remain ambiguous and their prevalence unclear. Here, we investigated the gene cluster responsible for inositol lipid synthesis in BT using a novel strain with inducible control of sphingolipid synthesis. We characterized the biosynthetic pathway from myo-inositol-phosphate (MIP) synthesis to phosphoinositol-dihydroceramide, including structural and kinetic studies of the enzyme MIP synthase (MIPS). We determined the crystal structure of recombinant BT MIPS with bound NAD cofactor at 2.0 Å resolution, and identified the first reported phosphatase for the conversion of bacterially-derived phosphatidylinositol phosphate (PIP) to phosphatidylinositol (PI). Transcriptomic analysis indicated inositol production is nonessential but its loss alters BT capsule expression. Bioinformatic and lipidomic comparisons of Bacteroidetes species revealed a novel second putative pathway for bacterial PI synthesis without a PIP intermediate. Our results indicate that inositol sphingolipid production, via one of the two pathways, is widespread in host-associated Bacteroidetes, and may be implicated in host interactions both indirectly via the capsule and directly through inositol lipid provisioning.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted April 27, 2021.
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Inositol lipid synthesis is widespread in host-associated Bacteroidetes
S. L. Heaver, H. H. Le, P. Tang, A. Baslé, J. Marles-Wright, E. L. Johnson, D. J. Campopiano, R. E. Ley
bioRxiv 2021.04.26.441525; doi: https://doi.org/10.1101/2021.04.26.441525
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Inositol lipid synthesis is widespread in host-associated Bacteroidetes
S. L. Heaver, H. H. Le, P. Tang, A. Baslé, J. Marles-Wright, E. L. Johnson, D. J. Campopiano, R. E. Ley
bioRxiv 2021.04.26.441525; doi: https://doi.org/10.1101/2021.04.26.441525

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