Succinate Dehydrogenase-Regulated Phosphoenolpyruvate Carboxykinase Sustains Copulation Fitness in Aging C. elegans Males

• Published in: iScience Vol. 23; no. 4; p. 100990
• Main Authors: Goncalves, Jimmy, Wan, Yufeng, Guo, Xiaoyan, Rha, Kyoungsun, LeBoeuf, Brigitte, Zhang, Liusuo, Estler, Kerolayne, Garcia, L. René
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 24.04.2020; Elsevier
• Subjects: Animal Physiology; Behavior Genetics; Biological Sciences; Biological Sciences; Animal Physiology; Behavior Genetics
• ISSN: 2589-0042; 2589-0042
• DOI: 10.1016/j.isci.2020.100990

Dysregulated metabolism accelerates reduced decision-making and locomotor ability during aging. To identify mechanisms for delaying behavioral decline, we investigated how C. elegans males sustain their copulatory behavior during early to mid-adulthood. We found that in mid-aged males, gluco-/glyceroneogenesis, promoted by phosphoenolpyruvate carboxykinase (PEPCK), sustains competitive reproductive behavior. C. elegans' PEPCK paralogs, pck-1 and pck-2, increase in expression during the first 2 days of adulthood. Insufficient PEPCK expression correlates with reduced egl-2-encoded ether-a-go-go K+ channel expression and premature hyper-excitability of copulatory circuits. For copulation, pck-1 is required in neurons, whereas pck-2 is required in the epidermis. However, PCK-2 is more essential, because we found that epidermal PCK-2 likely supplements the copulation circuitry with fuel. We identified the subunit A of succinate dehydrogenase SDHA-1 as a potent modulator of PEPCK expression. We postulate that during mid-adulthood, reduction in mitochondrial physiology signals the upregulation of cytosolic PEPCK to sustain the male's energy demands. [Display omitted] •C. elegans upregulates pck-1- and pck-2-encoded PEPCK during early adulthood•Loss of PEPCK causes premature male copulatory behavior decline•Epidermal PEPCK is required to sustain the copulatory fitness•Subunit A of succinate dehydrogenase antagonizes PEPCK expression Biological Sciences; Animal Physiology; Behavior Genetics