Conversion of dietary inositol into propionate and acetate by commensal Anaerostipes associates with host health

Thi Phuong Nam Bui; Louise Mannerås-Holm; Robert Puschmann; Hao Wu; Antonio Dario Troise; Bart Nijsse; Sjef Boeren; Fredrik Bäckhed; Dorothea Fiedler; Willem M. deVos

doi:10.1038/s41467-021-25081-w

Conversion of dietary inositol into propionate and acetate by commensal Anaerostipes associates with host health

Thi Phuong Nam Bui^*, Louise Mannerås-Holm, Robert Puschmann, Hao Wu, Antonio Dario Troise, Bart Nijsse, Sjef Boeren, Fredrik Bäckhed, Dorothea Fiedler, Willem M. deVos

^*Corresponding author af dette arbejde

Bäckhed Group

Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › peer review

162 Citationer (Scopus)

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Abstract

We describe the anaerobic conversion of inositol stereoisomers to propionate and acetate by the abundant intestinal genus Anaerostipes. A inositol pathway was elucidated by nuclear magnetic resonance using [¹³C]-inositols, mass spectrometry and proteogenomic analyses in A. rhamnosivorans, identifying 3-oxoacid CoA transferase as a key enzyme involved in both 3-oxopropionyl-CoA and propionate formation. This pathway also allowed conversion of phytate-derived inositol into propionate as shown with [¹³C]-phytate in fecal samples amended with A. rhamnosivorans. Metabolic and (meta)genomic analyses explained the adaptation of Anaerostipes spp. to inositol-containing substrates and identified a propionate-production gene cluster to be inversely associated with metabolic biomarkers in (pre)diabetes cohorts. Co-administration of myo-inositol with live A. rhamnosivorans in western-diet fed mice reduced fasting-glucose levels comparing to heat-killed A. rhamnosivorans after 6-weeks treatment. Altogether, these data suggest a potential beneficial role for intestinal Anaerostipes spp. in promoting host health.

Originalsprog	Engelsk
Artikelnummer	4798
Tidsskrift	Nature Communications
Vol/bind	12
Udgave nummer	1
Antal sider	16
ISSN	2041-1723
DOI	https://doi.org/10.1038/s41467-021-25081-w
Status	Udgivet - 2021

Bibliografisk note

Funding Information:
This work was partially supported by the SIAM Gravitation Grant 024.002.002 and Spinoza Award of the Netherlands Organization for Scientific Research to WMdV as well as Caelus Pharmaceuticals B.V. Authors acknowledge Jarmo Ritari & Lars Paulin for their assistance for genome sequencing, Daan Vliet for his assistance in genome submission and Tatiana Nikolaeva for technical support for NMR analysis; Andrea for advice on LC-MS analysis; Anna Hallén for the assistance in gavage treatments in the mice.

Publisher Copyright:
© 2021, The Author(s).

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Conversion of dietary inositol into propionate and acetate by commensal Anaerostipes associates with host healthForlagets udgivne version, 2,67 MBLicens: CC BY

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abstract = "We describe the anaerobic conversion of inositol stereoisomers to propionate and acetate by the abundant intestinal genus Anaerostipes. A inositol pathway was elucidated by nuclear magnetic resonance using [13C]-inositols, mass spectrometry and proteogenomic analyses in A. rhamnosivorans, identifying 3-oxoacid CoA transferase as a key enzyme involved in both 3-oxopropionyl-CoA and propionate formation. This pathway also allowed conversion of phytate-derived inositol into propionate as shown with [13C]-phytate in fecal samples amended with A. rhamnosivorans. Metabolic and (meta)genomic analyses explained the adaptation of Anaerostipes spp. to inositol-containing substrates and identified a propionate-production gene cluster to be inversely associated with metabolic biomarkers in (pre)diabetes cohorts. Co-administration of myo-inositol with live A. rhamnosivorans in western-diet fed mice reduced fasting-glucose levels comparing to heat-killed A. rhamnosivorans after 6-weeks treatment. Altogether, these data suggest a potential beneficial role for intestinal Anaerostipes spp. in promoting host health.",

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AU - Bui, Thi Phuong Nam

AU - Mannerås-Holm, Louise

AU - Puschmann, Robert

AU - Wu, Hao

AU - Troise, Antonio Dario

AU - Nijsse, Bart

AU - Boeren, Sjef

AU - Bäckhed, Fredrik

AU - Fiedler, Dorothea

AU - deVos, Willem M.

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N2 - We describe the anaerobic conversion of inositol stereoisomers to propionate and acetate by the abundant intestinal genus Anaerostipes. A inositol pathway was elucidated by nuclear magnetic resonance using [13C]-inositols, mass spectrometry and proteogenomic analyses in A. rhamnosivorans, identifying 3-oxoacid CoA transferase as a key enzyme involved in both 3-oxopropionyl-CoA and propionate formation. This pathway also allowed conversion of phytate-derived inositol into propionate as shown with [13C]-phytate in fecal samples amended with A. rhamnosivorans. Metabolic and (meta)genomic analyses explained the adaptation of Anaerostipes spp. to inositol-containing substrates and identified a propionate-production gene cluster to be inversely associated with metabolic biomarkers in (pre)diabetes cohorts. Co-administration of myo-inositol with live A. rhamnosivorans in western-diet fed mice reduced fasting-glucose levels comparing to heat-killed A. rhamnosivorans after 6-weeks treatment. Altogether, these data suggest a potential beneficial role for intestinal Anaerostipes spp. in promoting host health.

AB - We describe the anaerobic conversion of inositol stereoisomers to propionate and acetate by the abundant intestinal genus Anaerostipes. A inositol pathway was elucidated by nuclear magnetic resonance using [13C]-inositols, mass spectrometry and proteogenomic analyses in A. rhamnosivorans, identifying 3-oxoacid CoA transferase as a key enzyme involved in both 3-oxopropionyl-CoA and propionate formation. This pathway also allowed conversion of phytate-derived inositol into propionate as shown with [13C]-phytate in fecal samples amended with A. rhamnosivorans. Metabolic and (meta)genomic analyses explained the adaptation of Anaerostipes spp. to inositol-containing substrates and identified a propionate-production gene cluster to be inversely associated with metabolic biomarkers in (pre)diabetes cohorts. Co-administration of myo-inositol with live A. rhamnosivorans in western-diet fed mice reduced fasting-glucose levels comparing to heat-killed A. rhamnosivorans after 6-weeks treatment. Altogether, these data suggest a potential beneficial role for intestinal Anaerostipes spp. in promoting host health.

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