The target of rapamycin (TOR) protein exists in two structurally and functionally distinct multi-protein complexes, TOR complex 1 (TORC1) and TORC2. TORC2 is composed of TOR, Rictor, LST8, and Sin-1. TORC2 is the activating, hydrophobic motif (HM) kinase of AKT, but may also phosphorylate other AGC kinases such as PKC and serum- and glucocorticoid-induced kinase (SGK). In yeast and mammals, genetic inactivation of TORC2 is lethal. Thus, the physiologic significance of this kinase complex remains unknown in the context of the living animal. We identified mutations in the C. elegans homologue of the essential TORC2 component rictor in a forward genetic screen for increased body fat. rictor is critical for balancing energy utilization and storage, as mutants inappropriately store fat as triglyceride despite being growth delayed, small, short lived, and laying an attenuated brood. Although rictor is expressed in neurons, muscle, intestine, and pharynx, expression in the intestine is sufficient to rescue fat mass and whole animal growth. Out of a pool of growth-delayed mutants with high body fat, we also identified loss-of-function mutations in the sole C. elegans homologue of SGK,
sgk-1, which we found to be in a genetic pathway with rictor. Growth, lifespan, and reproductive defects of rictor mutants can be entirely explained by
sgk-1. Alternatively, the high fat phenotype of rictor is partially dependent upon
akt-1,
akt-2, and
sgk-1 as assessed by quantitative lipid biochemistry (solid phase chromatography and GC/MS). Surprisingly, insulin-like signaling via insR/PI3K/FOXO is not the input to or output of TORC2, since
daf-2 (insR),
daf-18 (PTEN), and
daf-16 (FOXO) regulate fat mass in parallel to rictor. Thus, through as yet unidentified inputs and outputs, TORC2 signals through SGK-1 to regulate lifespan, growth, and reproduction, and through AKT and SGK to regulate fat metabolism. Genetic and genomic approaches identified numerous candidate signaling molecules that may participate in a genetic pathway with rictor regulating metabolism. Further, to begin to determine which nutrients might provide input directly or indirectly to TORC2, we took advantage of our observation that rictor mutants avoid a lawn of HB101, displaying phenotypes consistent with caloric restriction: slower growth, a further reduced body size, decreased energy expenditure, and extended lifespan. We have identified candidate bacterial genes and metabolic characteristics which cause rictor mutants to avoid HB101, giving insight as to how nutrients regulate metabolism and feeding behavior through TORC2.