Lysosomes are digestive organelles that govern cellular metabolism and homeostasis. Despite their importance to animal health and disease, the current model of lysosome structure and function is quite simplistic; autophagic lysosomes are thought to exist mainly as discrete vesicles with uniform activity. Here, we report that vesicular lysosomes in the C. elegans gut transform into an extensive, dynamic, tubular network in response to animal starvation. These tubular lysosomes (TLs) are acidic, serve as preferential sites of starvation-triggered autophagy, and are stimulated via inhibition of the mTOR pathway. Consistent with our past studies in flies, we identify
spin-1, a C. elegans Spinster ortholog, as a critical TL gene. Using an endogenously-tagged SPIN-1::Cherry transgenic line, we find that genetic models of caloric restriction show atypically high
spin-1 expression levels, which correlates with the constitutive presence of TLs throughout the gut. TLs also appear to contribute to the transgenerational effects of starvation; well-fed descendants of starved worms can show gut TLs for several generations. Notably, the presence of gut TLs in well-fed progeny is predictive of enhanced adult lifespan. Further, we find that experimental expression of the Drosophila TL stimulator SVIP in C. elegans is sufficient to induce gut TLs in well-fed worms and improve C. elegans health during aging. These findings highlight a new class of degradative lysosomes that act at the center of the cellular response to starvation, potentially coordinating its positive effects on animal health and longevity.