Resistance Development and Transcriptional Responses of Salmonella Enterica Strains to Bacteriophage Sf1 Treatment on Arabidopsis Thaliana

Abstract

This study explores the prevalence and mechanisms of in vitro and in planta phage resistance in Salmonella enterica, a critical concern for food safety. We examined three Salmonella Typhimurium strains, ST001, ST536, and ST580, that developed phage resistance on Arabidopsis plants. Strains ST001 and ST536 exhibited strong phage resistance and cross-resistance to heat, while ST580 was more susceptible, showing greater population declines and requiring a longer adaptation period. Interestingly, despite gaining phage resistance, all three strains became more sensitive to oxidative and acidic stressors, suggesting potential applications for food industry controls. RNA-seq analysis indicated diverse transcriptional responses to phage exposure: ST580 displayed significant gene expression changes, while ST001 and ST536 increased resistance through enhanced membrane protein synthesis and upregulated ribosome and membrane protein localization genes. ST001 also reduced O-antigen synthesis, blocking the SF1 phage receptor. These transcriptional trends were corroborated by phage attachment assays and membrane protein measurements, highlighting distinct adaptive mechanisms. Unlike ST001 and ST536, ST580’s resistance was inadequate to prevent phage adsorption, leading to more reactive transcriptional responses. This research underscores the complexity of phage-host interactions and reveals potential trade-offs, such as increased sensitivity to oxidative and acidic stresses. It offers insights into the dynamics of phage resistance, which could improve phage applications against foodborne pathogens, enhancing the efficacy and sustainability of phage-based safety interventions.

Keywords: Phage resistance, Salmonella enterica, RNA-seq, Cross-resistance, foodborne pathogens, Phage-host interactions