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Bacteria have evolved sophisticated antiphage systems that halt phage replication upon detecting specific phage triggers. Identifying phage triggers is crucial to our understanding of immune signalling; however, they are challenging to predict. Here we used a plasmid library that expressed over 400 phage protein-coding genes from 6 phages to identify triggers of known and undiscovered antiphage systems. We transformed our library into 39 diverse strains of E. coli. Each strain natively harbours a different suite of antiphage systems whose activation typically inhibits growth. By tracking plasmids that were selectively depleted, we identified over 100 candidate phage trigger-E. coli pairs. Two phage proteins were further investigated, revealing that T7 gp17 and additional tail fibre proteins activated the undescribed antiphage system PD-T2-1 and identifying that λ gpE major capsid protein activated the antiphage system Avs8. These experiments provide a unique dataset for the continued definition of the molecular mechanisms underlying the bacterial immune system.