Queuosine promotes wecB-dependent phage resistance and biofilm formation in marine bacterium Shewanella glacialimarina
Transfer RNA (tRNA) modifications critically fine-tune translational accuracy and efficiency, influencing bacterial adaptation to environmental challenges. Among these, the queuosine (Q) modification has recently emerged as a regulator of biofilm formation, yet its role during phage infection remains unknown. Here, we investigate how Q modification links host translational control to phage infection. We show that phage infection activates the Q biosynthetic pathway, leading to elevated Q levels and enhanced translation of NAT-biased genes. This shift drives two interconnected outcomes, namely increased biofilm formation and enhanced mutagenesis mediated by translesion synthesis polymerases. We further identify conserved, slippage-prone regions within surface-related genes that act as hotspots for adaptive variation. Together, our findings uncover a novel mechanistic link between tRNA modification and phage-driven bacterial diversification. AUTHOR SUMMARYTo survive changing environmental conditions, bacteria constantly adjust their metabolic processes, including how they translate their genetic information into proteins. One such adjustment mechanism involves carefully balancing the level of chemical modification on transfer RNA (tRNA), the key adapter molecule that carries amino acids but also regulates protein synthesis. In this study, we explore how a cold-active bacterium relies on queuosine, a wobble position tRNA modification, to mediate host cell responses to bacteriophage infection. We observe that as viral infection progresses, the bacterial host cells increase the level of queuosine modification present on tRNAs. This alters the efficiency by which specific proteins are produced, favoring those that are involved in biofilm synthesis and thereby form protective communities that help bacteria survive stress. At the same time, queuosine also promotes error-prone DNA replication processes that lead to an overall increase in bacterial mutation rates. Taken together, our results reveal how a small molecular change in tRNA can reshape bacterial responses to viral infection, ultimately driving genetic diversity and survival.