Metabolomic “Dark Matter” Dependent on Peroxisomal β-Oxidation in <i>Caenorhabditis elegans</i>

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

doi:10.1021/jacs.7b11811

Cited by 57 publications

(89 citation statements)

References 62 publications

(175 reference statements)

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“…1). By comparing molecular ion weights, mass spectrometry (MS)/MS spectra, and retention times with those of known ascarosides 10,29 , we determined that these additional peaks represent ascarosides with shorter side chains, specifically ascr#10, ascr#1, and ascr#9 ( Supplementary Figs. 2 and 3).…”

Section: Resultsmentioning

confidence: 99%

“…Mass spectrometric analysis. High-resolution LC-MS analysis was performed on a Dionex 3000 UPLC system coupled with a Thermo Q Exactive high-resolution mass spectrometer as described previously 10,46 . Metabolite extracts were separated using a water-acetonitrile gradient using Agilent ZORBOX Eclispse XDB-C18 rapid resolution column (2.1 × 150 mm, particle size 1.8-micron) maintained at 40°C…”

Section: Methodsmentioning

confidence: 99%

“…Nematodes are among the most abundant animals on earth 9 , and plant-parasitic nematodes are ubiquitous in soil and parasitize most commercial crops causing annual losses tens of billions of dollars. Ascarosides are glycosides of the dideoxysugar ascarylose that carry a fatty acid-derived lipophilic side chain and are optionally decorated with additional building blocks of diverse metabolic origin 10,11 (Fig. 1b).…”

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confidence: 99%

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Plant metabolism of nematode pheromones mediates plant-nematode interactions

et al. 2020

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Microorganisms and nematodes in the rhizosphere profoundly impact plant health, and small-molecule signaling is presumed to play a central role in plant rhizosphere interactions. However, the nature of the signals and underlying mechanisms are poorly understood. Here we show that the ascaroside ascr#18, a pheromone secreted by plant-parasitic nematodes, is metabolized by plants to generate chemical signals that repel nematodes and reduce infection. Comparative metabolomics of plant tissues and excretions revealed that ascr#18 is converted into shorter side-chained ascarosides that confer repellency. An Arabidopsis mutant defective in two peroxisomal acyl-CoA oxidases does not metabolize ascr#18 and does not repel nematodes, indicating that plants, like nematodes, employ conserved peroxisomal β-oxidation to edit ascarosides and change their message. Our results suggest that plant-editing of nematode pheromones serves as a defense mechanism that acts in parallel to conventional pattern-triggered immunity, demonstrating that plants may actively manipulate chemical signaling of soil organisms.

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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confidence: 99%

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Plant metabolism of nematode pheromones mediates plant-nematode interactions

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“…Like mitochondrial β-oxidation, peroxisomal β-oxidation catalyzes chain shortening of acyl-CoAs by four enzymatic steps yielding acetyl-CoA. Despite that peroxisomal βoxidation in C. elegans is mostly known for oxidizing very long-chain fatty acids (VLCFAs) and for the synthesis of ascarosides (Artyukhin et al, 2018), long-and medium chain saturated and unsaturated fatty acids can also serve as substrates for peroxisomal β-oxidation (Poirier, Antonenkov, Glumoff, & Hiltunen, 2006). The first step is catalyzed by the enzyme acyl-CoA oxidase (ACOX), considered to be the main regulator of the flux through the pathway.…”

Section: Survival Of the Hlh-30 Mutant During Starvation Is Dependentmentioning

confidence: 99%

HLH-30 dependent rewiring of metabolism during starvation in C. elegans

Dall

Havelund

Harvald

et al. 2020

Preprint

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SummaryOne of the most fundamental challenges for all living organisms is to sense and respond to alternating nutritional conditions in order to adapt their metabolism and physiology to promote survival and achieve balanced growth. Here, we applied metabolomics and lipidomics to examine temporal regulation of metabolism during starvation in wildtype Caenorhabditis elegans and in animals lacking the transcription factor HLH-30. Our findings show for the first time that starvation alters the abundance of hundreds of metabolites and lipid species in a temporal- and HLH-30-dependent manner. We demonstrate that premature death of hlh-30 animals under starvation can be prevented by supplementation of exogenous fatty acids, and that HLH-30 is required for complete oxidation of long-chain fatty acids. We further show that RNAi-mediated knockdown of the gene encoding carnitine palmitoyl transferase I (cpt-1) only impairs survival of wildtype animals and not of hlh-30 animals. Strikingly, we also find that compromised generation of peroxisomes by prx-5 knockdown renders hlh-30 animals hypersensitive to starvation, which cannot be rescued by supplementation of exogenous fatty acids. Collectively, our observations show that mitochondrial functions are compromised in hlh-30 animals and that hlh-30 animals rewire their metabolism to largely depend on functional peroxisomes during starvation, underlining the importance of metabolic plasticity to maintain survival.Abstract Figure

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“…daf-22 worms fail to produce hundreds of metabolites, not only ascarosides (Artyukhin et al 2018). For this reason tested whether exposing parents to a synthetic blend of major ascarosides (#2,#3) would induce a relative germline delay in progeny.…”

Section: Exposure Of Parents To Ascarosides Is Sufficient To Induce Gmentioning

confidence: 99%

Neuronal perception of the social environment intergenerationally controls germline development and generation time inC. elegans

Perez

Shamalnasab

Mata‐Cabana

et al. 2020

Preprint

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An old and controversial question in biology is whether information perceived by the nervous system of an animal can ‘cross the Weismann barrier’ to alter the phenotypes and fitness of their progeny. Here we show that such intergenerational transmission of sensory information occurs in the model organism, C. elegans, with a major effect on fitness. Specifically, that perception of social pheromones by chemosensory neurons controls the post-embryonic timing of development of one tissue – the germline – relative to others in an animal’s progeny. Neuronal perception of the social environment thus intergenerationally controls the generation time of this animal.

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

Cited by 57 publications

References 62 publications

Plant metabolism of nematode pheromones mediates plant-nematode interactions

Plant metabolism of nematode pheromones mediates plant-nematode interactions

HLH-30 dependent rewiring of metabolism during starvation in C. elegans

Neuronal perception of the social environment intergenerationally controls germline development and generation time inC. elegans

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