Dataset Information

Transgenerational fitness effects of lifespan extension by dietary restriction in Caenorhabditis elegans.

ABSTRACT: Dietary restriction (DR) increases lifespan in a broad variety of organisms and improves health in humans. However, long-term transgenerational consequences of dietary interventions are poorly understood. Here, we investigated the effect of DR by temporary fasting (TF) on mortality risk, age-specific reproduction and fitness across three generations of descendants in Caenorhabditis elegans. We show that while TF robustly reduces mortality risk and improves late-life reproduction of the individuals subject to TF (P₀), it has a wide range of both positive and negative effects on their descendants (F₁-F₃). Remarkably, great-grandparental exposure to TF in early life reduces fitness and increases mortality risk of F₃ descendants to such an extent that TF no longer promotes a lifespan extension. These findings reveal that transgenerational trade-offs accompany the instant benefits of DR, underscoring the need to consider fitness of future generations in pursuit of healthy ageing.

SUBMITTER: Ivimey-Cook ER

PROVIDER: S-EPMC8113902 | biostudies-literature | 2021 May

REPOSITORIES: biostudies-literature

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Transgenerational fitness effects of lifespan extension by dietary restriction in <i>Caenorhabditis elegans</i>.

Ivimey-Cook Edward R ER Sales Kris K Carlsson Hanne H Immler Simone S Chapman Tracey T Maklakov Alexei A AA

Proceedings. Biological sciences 20210512 1950

Dietary restriction (DR) increases lifespan in a broad variety of organisms and improves health in humans. However, long-term transgenerational consequences of dietary interventions are poorly understood. Here, we investigated the effect of DR by temporary fasting (TF) on mortality risk, age-specific reproduction and fitness across three generations of descendants in <i>Caenorhabditis elegans</i>. We show that while TF robustly reduces mortality risk and improves late-life reproduction of the in ...[more]

PMID: 33975472

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Project description:BackgroundA healthy microbiome influences host physiology through a mutualistic relationship, which can be important for the host to cope with cellular stress by promoting fitness and survival. The mammalian microbiome is highly complex and attributing host phenotypes to a specific member of the microbiome can be difficult. The model organism Caenorhabditis elegans and its native microbiome, discovered recently, can serve as a more tractable, experimental model system to study host-microbiome interactions. In this study, we investigated whether certain members of C. elegans native microbiome would offer a benefit to their host and putative molecular mechanisms using a combination of phenotype screening, omics profiling and functional validation.ResultsA total of 16 members of C. elegans microbiome were screened under chemically-induced toxicity. Worms grown with Chryseobacterium sp. CHNTR56 MYb120 or Comamonas sp. 12022 MYb131, were most resistant to oxidative chemical stress (SiO2 nanoparticles and juglone), as measured by progeny output. Further investigation showed that Chryseobacterium sp. CHNTR56 positively influenced the worm's lifespan, whereas the combination of both isolates had a synergistic effect. RNAseq analysis of young adult worms, grown with either isolate, revealed the enrichment of cellular detoxification mechanisms (glutathione metabolism, drug metabolism and metabolism of xenobiotics) and signaling pathways (TGF-beta and Wnt signaling pathways). Upregulation of cysteine synthases (cysl genes) in the worms, associated with glutathione metabolism, was also observed. Nanopore sequencing uncovered that the genomes of the two isolates have evolved to favor the specific route of the de novo synthesis pathway of vitamin B6 (cofactor of cysl enzymes) through serC or pdxA2 homologs. Finally, co-culture with vitamin B6 extended worm lifespan.ConclusionsIn summary, our study indicates that certain colonizing members of C. elegans have genomic diversity in vitamin B6 synthesis and promote host fitness and lifespan extension. The regulation of host cellular detoxification genes (i.e. gst) along with cysl genes at the transcriptome level and the bacterium-specific vitamin B6 synthesis mechanism at the genome level are in an agreement with enhanced host glutathione-based cellular detoxification due to this interspecies relationship. C. elegans is therefore a promising alternative model to study host-microbiome interactions in host fitness and lifespan.

Dataset Information

Transgenerational fitness effects of lifespan extension by dietary restriction in Caenorhabditis elegans.

Publications

Transgenerational fitness effects of lifespan extension by dietary restriction in <i>Caenorhabditis elegans</i>.

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