Selective autophagy of ribosomes balances a tradeoff between starvation survival and growth resumption

Abstract

In environments with fluctuating nutrient abundance, organisms must survive periods of starvation, yet quickly resume growth upon food encounter. A tradeoff between these objectives is well-documented in microbes, where it is caused by the need to partition the total cellular protein content between growth- and survival-enhancing proteins. However, the molecular mechanisms of growth-survival tradeoffs in multicellular animals remain largely unknown. Here, we addressed this mechanism for C. elegans by measuring the dynamic changes of its proteome during starvation using live imaging and proteomics. We found that starved animals catabolize ribosomal proteins through autophagy, which provides essential energy for survival while preserving organismal integrity. However, the resulting decline in ribosomes delayed growth resumption upon refeeding until pre-starvation ribosome levels were restored. Genetic inhibition of ribosomal autophagy had a dual effect: although it accelerated growth after short starvation, it compromised survival during prolonged starvation. These findings reveal the rate of ribosomal catabolism as a key determinant of a tradeoff between starvation survival and rapid growth resumption whose tuning may adapt animals to different starvation durations. Our research shows how the need to balance protein allocation between growth and survival constrains animal physiology, highlighting the mechanistic role of proteome resource limitation in whole-organism tradeoffs.