Queuosine modification mediates cold-active growth in Shewanella glacialimarina

Efficient protein synthesis in cold-active bacteria requires precise coordination within the translation machinery to overcome the kinetic challenges imposed by growth at near-freezing temperatures (< 5 {degrees}C). Post-transcriptional modifications (PTMs) on transfer RNA (tRNA)--particularly those located at the wobble position 34--are central to this coordination as they regulate decoding speed and fidelity. Here, we show that queuosine (Q) modification in the cold-active marine bacterium Shewanella glacialimarina TZS-4T is dynamically regulated in response to bacterial growth and environmental conditions. Importantly, we demonstrate that Q levels are modulated in a tRNA isoacceptor-specific manner during cold-active growth, while Q-deficiency produces a cold-sensitive phenotype that underscores the functional importance of Q modification. Proteomic analysis of the Q-deficient {Delta}tgt mutant revealed that tRNAHis Q-hypomodification activates the histidine biosynthesis pathway, whereas the concomitant phosphate-starvation-like response reflects a general consequence of global disruption of Q-modified tRNAs. Consequently, we propose a model where Q modification maintains efficient codon decoding and protein quality control at near-freezing temperatures, whereas loss of Q destabilizes codon decoding and ultimately compromises protein homeostasis.