An excreted small molecule promotes C. elegans reproductive development and aging

Ludewig, Andreas H.; Artyukhin, Alexander B.; Aprison, Erin Z.; Rodrigues, Pedro Reis; Pulido, Dania C.; Burkhardt, Russell N.; Panda, Oishika; Zhang, Ying K.; Gudibanda, Pooja; Ruvinsky, Ilya; Schroeder, Frank C.

doi:10.1038/s41589-019-0321-7

Cited by 44 publications

(66 citation statements)

References 55 publications

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“…Thus, the biosynthesis of ascarosides and other C. elegans signaling molecules (e.g. nacq#1) ( Ludewig et al, 2019 ) represents a fascinating model system for the endogenous regulation of inter-organismal small-molecule signaling in metazoans. However, for most of the >200 recently identified C. elegans metabolites ( Artyukhin et al, 2018 ; von Reuss et al, 2012 ; Artyukhin et al, 2013 ), biosynthetic knowledge is sparse.…”

Section: Introductionmentioning

confidence: 99%

Modular metabolite assembly in Caenorhabditis elegans depends on carboxylesterases and formation of lysosome-related organelles

Wrobel

Cohen

et al. 2020

eLife

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Signaling molecules derived from attachment of diverse metabolic building blocks to ascarosides play a central role in the life history of C. elegans and other nematodes; however, many aspects of their biogenesis remain unclear. Using comparative metabolomics, we show that a pathway mediating formation of intestinal lysosome-related organelles (LROs) is required for biosynthesis of most modular ascarosides as well as previously undescribed modular glucosides. Similar to modular ascarosides, the modular glucosides are derived from highly selective assembly of moieties from nucleoside, amino acid, neurotransmitter, and lipid metabolism, suggesting that modular glucosides, like the ascarosides, may serve signaling functions. We further show that carboxylesterases that localize to intestinal organelles are required for the assembly of both modular ascarosides and glucosides via ester and amide linkages. Further exploration of LRO function and carboxylesterase homologs in C. elegans and other animals may reveal additional new compound families and signaling paradigms.

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Section: Introductionmentioning

confidence: 99%

Modular metabolite assembly in Caenorhabditis elegans depends on carboxylesterases and formation of lysosome-related organelles

Wrobel

Cohen

et al. 2020

eLife

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“…Thus, the biosynthesis of ascarosides and other C. elegans signaling molecules (e.g. nacq#1) 15 represents a fascinating model system for the endogenous regulation of inter- organismal small-molecule signaling in metazoans. However, for most of the >200 recently identified C. elegans metabolites 2, 8, 9 , biosynthetic knowledge is sparse.…”

Section: Introductionmentioning

confidence: 99%

Modular metabolite assembly in C. elegans depends on carboxylesterases and formation of lysosome-related organelles

Wrobel

Cohen

et al. 2020

Preprint

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Signaling molecules derived from attachment of diverse primary metabolic building blocks to ascarosides play a central role in the life history of C. elegans and other nematodes; however, many aspects of their biogenesis remain unclear. Using comparative metabolomics, we show that lysosome-related organelles (LROs) are required for biosynthesis of most modular ascarosides as well as previously undescribed modular glucosides. Both modular glucosides and ascarosides are derived from highly selective assembly of moieties from nucleoside, amino acid, neurotransmitter, and lipid metabolism. We further show that cholinesterase (cest) homologs that localize to the LROs are required for assembly of both modular ascarosides and glucosides, mediating formation of ester and amide linkages between subsets of building blocks. Their specific biosynthesis suggests that modular glucosides, like ascarosides, serve dedicated signaling functions. Further exploration of LRO function and cest homologs in C. elegans and other animals may reveal additional new compound families and signaling paradigms.Abstract Figure

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“…The metabolites of C. elegans mainly contain organic acids, amino acids, sugars and pheromones, and some of these metabolites have been con rmed to regulate the development and social behaviors of nematodes (Kaplan et al 2009; Reilly and Srinivasan 2019). For example, nacq#1, which is an N-acylated glutamine, could promote onset of sexual maturity of C. elegans hermaphrodites (Ludewig et al 2019). Ascarosides, the pheromone secreted by plant-parasitic nematodes, can be recognized by plants to modify their immune system to reduce infection (Manohar et al 2020).…”

Section: Resultsmentioning

confidence: 99%

“…DiscussionBacterial-feeding nematodes metabolites promote bacterial IAA synthesis Understanding the extremely complex interactions between soil fauna and microorganisms is important to explore how soil ecosystems function and maintain stability(Huang et al 2019;Ludewig et al 2019; …”

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confidence: 99%

Metabolites of Bacterial-Feeding Nematodes Stimulate Bacterial Indole-3-Acetic Acid (IAA) Synthesis

Li¹,

Li²,

Zhou³

et al. 2020

Preprint

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Interorganismal metabolites play significant roles in regulating behaviors and communications between organisms. Nematodes are the most abundant animals on earth, and function well in soil ecosystem due to their interactions with microbes. Bacterial-feeding nematodes stimulate the activity of indole-3-acetic acid (IAA)-producing bacteria and increase the content of IAA in soil. However, we do not fully understand how bacterial-feeding nematodes interact with bacteria and affect IAA synthesis. In this study, the model nematode Caenorhabditis elegans and three species of soil-dwelling IAA-producing bacteria ( Bacillus amyloliquefaciens JX1, Arthrobacter pascens ZZ21 and A. chlorphenolicus L4) were employed to determine the effect of nematodes on the IAA biosynthesis of bacteria. Then the metabolites and extracts of C. elegans were tested the effect on three bacterial IAA synthesis (but only A. pascens ZZ21 for the extracts). Lastly, two soil-dwelling bacterial-feeding nematodes ( Mesorhabditis sp. and Acrobeloides sp.) and two IAA-producing bacteria ( B. amyloliquefaciens JX1 and A. pascens ZZ21) were subsequently used to explore the universality of this interaction. Our results showed that the metabolites or extracts of nematodes could promote the IAA biosynthesis of IAA-producing bacteria, and implied this stimulatory effect maybe widely spread in metabolites of bacterial-feeding nematodes and IAA-producing bacteria, but vary with nematodes and bacteria species. Our findings indicate that bacterial-feeding nematodes could mediate the interaction between nematodes and bacteria by their metabolites, except for their feeding behavior, and offer insights into the ecological function of the metabolites of nematodes.

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An excreted small molecule promotes C. elegans reproductive development and aging

Cited by 44 publications

References 55 publications

Modular metabolite assembly in Caenorhabditis elegans depends on carboxylesterases and formation of lysosome-related organelles

Modular metabolite assembly in Caenorhabditis elegans depends on carboxylesterases and formation of lysosome-related organelles

Modular metabolite assembly in C. elegans depends on carboxylesterases and formation of lysosome-related organelles

Metabolites of Bacterial-Feeding Nematodes Stimulate Bacterial Indole-3-Acetic Acid (IAA) Synthesis

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