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Article ; Online: Comparative metabolomics with Metaboseek reveals functions of a conserved fat metabolism pathway in C. elegans.

Helf, Maximilian J / Fox, Bennett W / Artyukhin, Alexander B / Zhang, Ying K / Schroeder, Frank C

2022 Volume 13, Issue 1, Page(s) 782

Abstract: Untargeted metabolomics via high-resolution mass spectrometry can reveal more than 100,000 molecular features in a single sample, many of which may represent unidentified metabolites, posing significant challenges to data analysis. We here introduce ... ...

Abstract	Untargeted metabolomics via high-resolution mass spectrometry can reveal more than 100,000 molecular features in a single sample, many of which may represent unidentified metabolites, posing significant challenges to data analysis. We here introduce Metaboseek, an open-source analysis platform designed for untargeted comparative metabolomics and demonstrate its utility by uncovering biosynthetic functions of a conserved fat metabolism pathway, α-oxidation, using C. elegans as a model. Metaboseek integrates modules for molecular feature detection, statistics, molecular formula prediction, and fragmentation analysis, which uncovers more than 200 previously uncharacterized α-oxidation-dependent metabolites in an untargeted comparison of wildtype and α-oxidation-defective hacl-1 mutants. The identified metabolites support the predicted enzymatic function of HACL-1 and reveal that α-oxidation participates in metabolism of endogenous β-methyl-branched fatty acids and food-derived cyclopropane lipids. Our results showcase compound discovery and feature annotation at scale via untargeted comparative metabolomics applied to a conserved primary metabolic pathway and suggest a model for the metabolism of cyclopropane lipids.
MeSH term(s)	Animals ; Caenorhabditis elegans/genetics ; Caenorhabditis elegans/metabolism ; Carbon-Carbon Lyases/genetics ; Carbon-Carbon Lyases/metabolism ; Fatty Acids/genetics ; Fatty Acids/metabolism ; Humans ; Larva ; Lipid Metabolism/genetics ; Mass Spectrometry ; Metabolic Networks and Pathways/genetics ; Metabolome ; Metabolomics/methods ; Oxidation-Reduction
Chemical Substances	Fatty Acids ; Carbon-Carbon Lyases (EC 4.1.-)
Language	English
Publishing date	2022-02-10
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-022-28391-9
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Evolutionarily related host and microbial pathways regulate fat desaturation in C. elegans.

Fox, Bennett W / Helf, Maximilian J / Burkhardt, Russell N / Artyukhin, Alexander B / Curtis, Brian J / Palomino, Diana Fajardo / Schroeder, Allen F / Chaturbedi, Amaresh / Tauffenberger, Arnaud / Wrobel, Chester J J / Zhang, Ying K / Lee, Siu Sylvia / Schroeder, Frank C

Nature communications

2024 Volume 15, Issue 1, Page(s) 1520

Abstract: Fatty acid desaturation is central to metazoan lipid metabolism and provides building blocks of membrane lipids and precursors of diverse signaling molecules. Nutritional conditions and associated microbiota regulate desaturase expression, but the ... ...

Abstract	Fatty acid desaturation is central to metazoan lipid metabolism and provides building blocks of membrane lipids and precursors of diverse signaling molecules. Nutritional conditions and associated microbiota regulate desaturase expression, but the underlying mechanisms have remained unclear. Here, we show that endogenous and microbiota-dependent small molecule signals promote lipid desaturation via the nuclear receptor NHR-49/PPARα in C. elegans. Untargeted metabolomics of a β-oxidation mutant, acdh-11, in which expression of the stearoyl-CoA desaturase FAT-7/SCD1 is constitutively increased, revealed accumulation of a β-cyclopropyl fatty acid, becyp#1, that potently activates fat-7 expression via NHR-49. Biosynthesis of becyp#1 is strictly dependent on expression of cyclopropane synthase by associated bacteria, e.g., E. coli. Screening for structurally related endogenous metabolites revealed a β-methyl fatty acid, bemeth#1, which mimics the activity of microbiota-dependent becyp#1 but is derived from a methyltransferase, fcmt-1, that is conserved across Nematoda and likely originates from bacterial cyclopropane synthase via ancient horizontal gene transfer. Activation of fat-7 expression by these structurally similar metabolites is controlled by distinct mechanisms, as microbiota-dependent becyp#1 is metabolized by a dedicated β-oxidation pathway, while the endogenous bemeth#1 is metabolized via α-oxidation. Collectively, we demonstrate that evolutionarily related biosynthetic pathways in metazoan host and associated microbiota converge on NHR-49/PPARα to regulate fat desaturation.
MeSH term(s)	Animals ; Caenorhabditis elegans/metabolism ; Caenorhabditis elegans Proteins/metabolism ; PPAR alpha/metabolism ; Escherichia coli/genetics ; Escherichia coli/metabolism ; Fatty Acids/metabolism ; Cyclopropanes/metabolism
Chemical Substances	Caenorhabditis elegans Proteins ; PPAR alpha ; Fatty Acids ; Cyclopropanes
Language	English
Publishing date	2024-02-19
Publishing country	England
Document type	Journal Article
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-024-45782-2
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Evolutionarily related host and microbial pathways regulate fat desaturation.

Fox, Bennett W / Helf, Maximilian J / Burkhardt, Russell N / Artyukhin, Alexander B / Curtis, Brian J / Palomino, Diana Fajardo / Chaturbedi, Amaresh / Tauffenberger, Arnaud / Wrobel, Chester J J / Zhang, Ying K / Lee, Siu Sylvia / Schroeder, Frank C

bioRxiv : the preprint server for biology

2023

Abstract	Fatty acid desaturation is central to metazoan lipid metabolism and provides building blocks of membrane lipids and precursors of diverse signaling molecules. Nutritional conditions and associated microbiota regulate desaturase expression
Language	English
Publishing date	2023-08-31
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.08.31.555782
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Article ; Online: Photoaffinity probes for nematode pheromone receptor identification.

Zhang, Ying K / Reilly, Douglas K / Yu, Jingfang / Srinivasan, Jagan / Schroeder, Frank C

Organic & biomolecular chemistry

2019 Volume 18, Issue 1, Page(s) 36–40

Abstract: Identification of pheromone receptors plays a central role for uncovering signaling pathways that underlie chemical communication in animals. Here, we describe the synthesis and bioactivity of photoaffinity probes for the ascaroside ascr#8, a sex- ... ...

Abstract	Identification of pheromone receptors plays a central role for uncovering signaling pathways that underlie chemical communication in animals. Here, we describe the synthesis and bioactivity of photoaffinity probes for the ascaroside ascr#8, a sex-pheromone of the model nematode, Caenorhabditis elegans. Structure-activity studies guided incorporation of alkyne- and diazirine-moieties and revealed that addition of functionality in the sidechain of ascr#8 was well tolerated, whereas modifications to the ascarylose moiety resulted in loss of biological activity. Our study will guide future probe design and provides a basis for pheromone receptor identification via photoaffinity labeling in C. elegans.
MeSH term(s)	Animals ; Caenorhabditis elegans/chemistry ; Molecular Structure ; Nematoda/chemistry ; Photoaffinity Labels/chemical synthesis ; Photoaffinity Labels/chemistry ; Receptors, Pheromone/analysis ; Receptors, Pheromone/metabolism
Chemical Substances	Photoaffinity Labels ; Receptors, Pheromone
Language	English
Publishing date	2019-11-26
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2097583-1
ISSN	1477-0539 ; 1477-0520
ISSN (online)	1477-0539
ISSN	1477-0520
DOI	10.1039/c9ob02099c
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Metabolomic “Dark Matter” Dependent on Peroxisomal β-Oxidation in Caenorhabditis elegans

Artyukhin, Alexander B / Zhang, Ying K / Akagi, Allison E / Panda, Oishika / Sternberg, Paul W / Schroeder, Frank C

Journal of the American Chemical Society. 2018 Feb. 28, v. 140, no. 8

2018

Abstract: Peroxisomal β-oxidation (pβo) is a highly conserved fat metabolism pathway involved in the biosynthesis of diverse signaling molecules in animals and plants. In Caenorhabditis elegans, pβo is required for the biosynthesis of the ascarosides, signaling ... ...

Abstract	Peroxisomal β-oxidation (pβo) is a highly conserved fat metabolism pathway involved in the biosynthesis of diverse signaling molecules in animals and plants. In Caenorhabditis elegans, pβo is required for the biosynthesis of the ascarosides, signaling molecules that control development, lifespan, and behavior in this model organism. Via comparative mass spectrometric analysis of pβo mutants and wildtype, we show that pβo in C. elegans and the satellite model P. pacificus contributes to life stage-specific biosynthesis of several hundred previously unknown metabolites. The pβo-dependent portion of the metabolome is unexpectedly diverse, e.g., intersecting with nucleoside and neurotransmitter metabolism. Cell type-specific restoration of pβo in pβo-defective mutants further revealed that pβo-dependent submetabolomes differ between tissues. These results suggest that interactions of fat, nucleoside, and other primary metabolism pathways can generate structural diversity reminiscent of that arising from combinatorial strategies in microbial natural product biosynthesis.
Keywords	Caenorhabditis elegans ; animals ; beta oxidation ; biosynthesis ; longevity ; mass spectrometry ; metabolites ; metabolome ; models ; mutants ; neurotransmitters ; nucleosides ; plants (botany) ; satellites ; tissues
Language	English
Dates of publication	2018-0228
Size	p. 2841-2852.
Publishing place	American Chemical Society
Document type	Article
ZDB-ID	3155-0
ISSN	1520-5126 ; 0002-7863
ISSN (online)	1520-5126
ISSN	0002-7863
DOI	10.1021/jacs.7b11811
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Article ; Online: Nematode Signaling Molecules Are Extensively Metabolized by Animals, Plants, and Microorganisms.

Yu, Yan / Zhang, Ying K / Manohar, Murli / Artyukhin, Alexander B / Kumari, Anshu / Tenjo-Castano, Francisco J / Nguyen, Hung / Routray, Pratyush / Choe, Andrea / Klessig, Daniel F / Schroeder, Frank C

ACS chemical biology

2021 Volume 16, Issue 6, Page(s) 1050–1058

Abstract: Many bacterivorous and parasitic nematodes secrete signaling molecules called ascarosides that play a central role regulating their behavior and development. Combining stable-isotope labeling and mass spectrometry-based comparative metabolomics, here we ... ...

Abstract	Many bacterivorous and parasitic nematodes secrete signaling molecules called ascarosides that play a central role regulating their behavior and development. Combining stable-isotope labeling and mass spectrometry-based comparative metabolomics, here we show that ascarosides are taken up from the environment and metabolized by a wide range of phyla, including plants, fungi, bacteria, and mammals, as well as nematodes. In most tested eukaryotes and some bacteria, ascarosides are metabolized into derivatives with shortened fatty acid side chains, analogous to ascaroside biosynthesis in nematodes. In plants and
MeSH term(s)	Animals ; Bacteria/metabolism ; Caenorhabditis elegans/metabolism ; Glycolipids/metabolism ; Metabolomics ; Mice ; Plants/metabolism ; Rats ; Signal Transduction
Chemical Substances	Glycolipids ; ascaroside A (11002-15-6)
Language	English
Publishing date	2021-05-21
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ISSN	1554-8937
ISSN (online)	1554-8937
DOI	10.1021/acschembio.1c00217
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Molecular Determinants of the Regulation of Development and Metabolism by Neuronal eIF2α Phosphorylation in

Kulalert, Warakorn / Sadeeshkumar, Harini / Zhang, Ying K / Schroeder, Frank C / Kim, Dennis H

Genetics

2017 Volume 206, Issue 1, Page(s) 251–263

Abstract: Cell-nonautonomous effects of signaling in the nervous system of animals can influence diverse aspects of organismal physiology. We previously showed that phosphorylation of Ser49 of the α-subunit of eukaryotic translation initiation factor 2 (eIF2α) in ... ...

Abstract	Cell-nonautonomous effects of signaling in the nervous system of animals can influence diverse aspects of organismal physiology. We previously showed that phosphorylation of Ser49 of the α-subunit of eukaryotic translation initiation factor 2 (eIF2α) in two chemosensory neurons by PEK-1/PERK promotes entry of
MeSH term(s)	Animals ; Binding Sites ; Caenorhabditis elegans/genetics ; Caenorhabditis elegans/growth & development ; Eukaryotic Initiation Factor-2/biosynthesis ; Eukaryotic Initiation Factor-2/genetics ; Eukaryotic Initiation Factor-2B/biosynthesis ; Eukaryotic Initiation Factor-2B/genetics ; Mutation ; Phosphorylation ; Protein Biosynthesis ; Sensory Receptor Cells/metabolism
Chemical Substances	Eukaryotic Initiation Factor-2 ; Eukaryotic Initiation Factor-2B
Language	English
Publishing date	2017-03-14
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2167-2
ISSN	1943-2631 ; 0016-6731
ISSN (online)	1943-2631
ISSN	0016-6731
DOI	10.1534/genetics.117.200568
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Improved Synthesis for Modular Ascarosides Uncovers Biological Activity.

Zhang, Ying K / Sanchez-Ayala, Marco A / Sternberg, Paul W / Srinivasan, Jagan / Schroeder, Frank C

Organic letters

2017 Volume 19, Issue 11, Page(s) 2837–2840

Abstract: A versatile synthesis of modular ascarosides, a family of signaling molecules from Caenorhabditis elegans and other nematodes, via hydrogenolysis of a cyclic sulfate derived from methyl-α-l-rhamnopyranoside is reported. The route enables selective ... ...

Abstract	A versatile synthesis of modular ascarosides, a family of signaling molecules from Caenorhabditis elegans and other nematodes, via hydrogenolysis of a cyclic sulfate derived from methyl-α-l-rhamnopyranoside is reported. The route enables selective introduction of different side chains at the 1, 2, and 4 positions of the sugar, as demonstrated for ascarosides from C. elegans and Pristionchus pacificus. Bioassays with synthetic samples of 4'-tigloyl ascaroside mbas#3 revealed its role as an avoidance or dispersal signal.
MeSH term(s)	Animals ; Caenorhabditis elegans ; Glycolipids/chemical synthesis ; Molecular Structure ; Pheromones
Chemical Substances	Glycolipids ; Pheromones
Language	English
Publishing date	2017-05-17
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	1523-7052
ISSN (online)	1523-7052
DOI	10.1021/acs.orglett.7b01009
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Improved Synthesis for Modular Ascarosides Uncovers Biological Activity

Zhang, Ying K / Sanchez-Ayala Marco A / Sternberg Paul W / Srinivasan Jagan / Schroeder Frank C

Organic letters. 2017 June 02, v. 19, no. 11

2017

Abstract: A versatile synthesis of modular ascarosides, a family of signaling molecules from Caenorhabditis elegans and other nematodes, via hydrogenolysis of a cyclic sulfate derived from methyl-Î±-l-rhamnopyranoside is reported. The route enables selective ... ...

Abstract	A versatile synthesis of modular ascarosides, a family of signaling molecules from Caenorhabditis elegans and other nematodes, via hydrogenolysis of a cyclic sulfate derived from methyl-Î±-l-rhamnopyranoside is reported. The route enables selective introduction of different side chains at the 1, 2, and 4 positions of the sugar, as demonstrated for ascarosides from C. elegans and Pristionchus pacificus. Bioassays with synthetic samples of 4â²-tigloyl ascaroside mbas#3 revealed its role as an avoidance or dispersal signal.
Keywords	Caenorhabditis elegans ; bioactive properties ; bioassays ; chemical reactions ; chemical structure ; organic compounds ; sugars ; sulfates
Language	English
Dates of publication	2017-0602
Size	p. 2837-2840.
Publishing place	American Chemical Society
Document type	Article
ISSN	1523-7052
DOI	10.1021%2Facs.orglett.7b01009
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Metabolomic "Dark Matter" Dependent on Peroxisomal β-Oxidation in Caenorhabditis elegans.

Artyukhin, Alexander B / Zhang, Ying K / Akagi, Allison E / Panda, Oishika / Sternberg, Paul W / Schroeder, Frank C

Journal of the American Chemical Society

2018 Volume 140, Issue 8, Page(s) 2841–2852

Abstract	Peroxisomal β-oxidation (pβo) is a highly conserved fat metabolism pathway involved in the biosynthesis of diverse signaling molecules in animals and plants. In Caenorhabditis elegans, pβo is required for the biosynthesis of the ascarosides, signaling molecules that control development, lifespan, and behavior in this model organism. Via comparative mass spectrometric analysis of pβo mutants and wildtype, we show that pβo in C. elegans and the satellite model P. pacificus contributes to life stage-specific biosynthesis of several hundred previously unknown metabolites. The pβo-dependent portion of the metabolome is unexpectedly diverse, e.g., intersecting with nucleoside and neurotransmitter metabolism. Cell type-specific restoration of pβo in pβo-defective mutants further revealed that pβo-dependent submetabolomes differ between tissues. These results suggest that interactions of fat, nucleoside, and other primary metabolism pathways can generate structural diversity reminiscent of that arising from combinatorial strategies in microbial natural product biosynthesis.
MeSH term(s)	Animals ; Caenorhabditis elegans/metabolism ; Glycolipids/biosynthesis ; Glycolipids/chemistry ; Metabolomics ; Molecular Structure ; Oxidation-Reduction ; Peroxisomes/metabolism
Chemical Substances	Glycolipids
Language	English
Publishing date	2018-02-16
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	3155-0
ISSN	1520-5126 ; 0002-7863
ISSN (online)	1520-5126
ISSN	0002-7863
DOI	10.1021/jacs.7b11811
Database	MEDical Literature Analysis and Retrieval System OnLINE

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