A dual-factor complex governs archaeal ribosome hibernation by sensing energy status

Abstract Efficient coupling of cellular energy status to ribosome regulation is fundamental for cellular survival. Here, we identify the Archaeal Ribosome regulatory Complex (ARC)—a previously uncharacterized dual-factor complex comprising ARC-P and ARC-A. Cryo-EM reveals that ARC anchors to the small ribosomal subunit, establishing a stringent blockade of the tRNA and mRNA paths via an electrostatic wedge mechanism. This hibernation state is modulated by energy status: the complex remains stably associated under low-energy conditions, whereas ATP binding triggers rapid mobilization. Genetic analyses demonstrate that ARC acts as a translational brake essential for preserving ribosomal structural integrity, with ARC-A serving as the primary inhibitory factor. Notably, while the loss of ARC accelerates growth, it impairs recovery in proportion to stress severity. Phylogenomic analysis identifies ARC as an evolutionarily novel and widely distributed dual-factor system, revealing a conserved regulatory strategy for metabolic-translational coupling across diverse archaea. Our findings define a fundamental strategy where modular complexes integrate metabolic sensing with mechanical sequestration to balance growth and persistence.