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The invertebrate Caenorhabditis elegans biosynthesizes ascorbate.

ABSTRACT: l-Ascorbate, commonly known as vitamin C, serves as an antioxidant and cofactor essential for many biological processes. Distinct ascorbate biosynthetic pathways have been established for animals and plants, but little is known about the presence or synthesis of this molecule in invertebrate species. We have investigated ascorbate metabolism in the nematode Caenorhabditis elegans, where this molecule would be expected to play roles in oxidative stress resistance and as cofactor in collagen and neurotransmitter synthesis. Using high-performance liquid chromatography and gas-chromatography mass spectrometry, we determined that ascorbate is present at low amounts in the egg stage, L1 larvae, and mixed animal populations, with the egg stage containing the highest concentrations. Incubating C. elegans with precursor molecules necessary for ascorbate synthesis in plants and animals did not significantly alter ascorbate levels. Furthermore, bioinformatic analyses did not support the presence in C. elegans of either the plant or the animal biosynthetic pathway. However, we observed the complete (13)C-labeling of ascorbate when C. elegans was grown with (13)C-labeled Escherichia coli as a food source. These results support the hypothesis that ascorbate biosynthesis in invertebrates may proceed by a novel pathway and lay the foundation for a broader understanding of its biological role.

SUBMITTER: Patananan AN

PROVIDER: S-EPMC4357563 | biostudies-literature | 2015 Mar

REPOSITORIES: biostudies-literature

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The invertebrate Caenorhabditis elegans biosynthesizes ascorbate.

Patananan Alexander N AN Budenholzer Lauren M LM Pedraza Maria E ME Torres Eric R ER Adler Lital N LN Clarke Steven G SG

Archives of biochemistry and biophysics 20150207

l-Ascorbate, commonly known as vitamin C, serves as an antioxidant and cofactor essential for many biological processes. Distinct ascorbate biosynthetic pathways have been established for animals and plants, but little is known about the presence or synthesis of this molecule in invertebrate species. We have investigated ascorbate metabolism in the nematode Caenorhabditis elegans, where this molecule would be expected to play roles in oxidative stress resistance and as cofactor in collagen and n ...[more]

PMID: 25668719

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Project description:BackgroundThe invertebrate immune system comprises physiological mechanisms, physical barriers and also behavioral responses. It is generally related to the vertebrate innate immune system and widely believed to provide nonspecific defense against pathogens, whereby the response to different pathogen types is usually mediated by distinct signalling cascades. Recent work suggests that invertebrate immune defense can be more specific at least at the phenotypic level. The underlying genetic mechanisms are as yet poorly understood.ResultsWe demonstrate in the model invertebrate Caenorhabditis elegans that a single gene, a homolog of the mammalian neuropeptide Y receptor gene, npr-1, mediates contrasting defense phenotypes towards two distinct pathogens, the Gram-positive Bacillus thuringiensis and the Gram-negative Pseudomonas aeruginosa. Our findings are based on combining quantitative trait loci (QTLs) analysis with functional genetic analysis and RNAseq-based transcriptomics. The QTL analysis focused on behavioral immune defense against B. thuringiensis, using recombinant inbred lines (RILs) and introgression lines (ILs). It revealed several defense QTLs, including one on chromosome X comprising the npr-1 gene. The wildtype N2 allele for the latter QTL was associated with reduced defense against B. thuringiensis and thus produced an opposite phenotype to that previously reported for the N2 npr-1 allele against P. aeruginosa. Analysis of npr-1 mutants confirmed these contrasting immune phenotypes for both avoidance behavior and nematode survival. Subsequent transcriptional profiling of C. elegans wildtype and npr-1 mutant suggested that npr-1 mediates defense against both pathogens through p38 MAPK signaling, insulin-like signaling, and C-type lectins. Importantly, increased defense towards P. aeruginosa seems to be additionally influenced through the induction of oxidative stress genes and activation of GATA transcription factors, while the repression of oxidative stress genes combined with activation of Ebox transcription factors appears to enhance susceptibility to B. thuringiensis.ConclusionsOur findings highlight the role of a single gene, npr-1, in fine-tuning nematode immune defense, showing the ability of the invertebrate immune system to produce highly specialized and potentially opposing immune responses via single regulatory genes.

Project description:The nematode Caenorhabditis elegans feeds on microbes in its natural environment. Some of these microbes are pathogenic and thus harmful to C. elegans. To minimize resulting fitness reductions, C. elegans has evolved various defence mechanisms including behavioural responses (e.g. avoidance behaviour) that reduce contact with the infectious microbes. In this study, we characterized the genetic architecture of natural variation in C. elegans avoidance behaviour against the infectious stages of the Gram-positive bacterium Bacillus thuringiensis. We performed an analysis of quantitative trait loci (QTLs) using recombinant inbred lines (RILs) and introgression lines (ILs) generated from a cross of two genetically as well as phenotypically distinct natural isolates N2 and CB4856. The analysis identified several QTLs that underlie variation in the behavioural response to pathogenic and/or non-pathogenic bacteria. One of the candidates is the npr-1 gene. This gene encodes a homolog of the mammalian neuropeptide receptor. Npr-1 was previously indicated to fully contribute to behavioural defence against the Gram-negative bacterium Pseudomonas aeruginosa and food patch-leaving behaviour on Escherichia coli. Interestingly, in our study, npr-1 is not the only gene mediating avoidance behaviour toward Bacillus thuringiensis. Moreover, our functional analyses show that npr-1 alleles appear to influence survival and avoidance behaviour toward Bacillus thuringiensis in exactly the opposite way than toward Pseudomonas aeruginosa. Our findings highlight the role of npr-1 in fine-tuning nematode behaviour in an ecological context depending on the microbe to which C. elegans is exposed. These opposite phenotypes reflect the diversity in innate immunity to pathogens. To understand the mechanism involved in these opposite phenotypes, we carried out a whole-genome transcriptomics study by RNA-Sequencing. This study includes two pathogens: Pseudomonas aeruginosa PA14 and Bacillus thuringiensis B-18247 (BT247), two strains: N2 and npr-1 (ur89), two time points (12 and 24h) and standard lab food E. coli OP50 as control.

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The invertebrate Caenorhabditis elegans biosynthesizes ascorbate.

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The invertebrate Caenorhabditis elegans biosynthesizes ascorbate.

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