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By repairing oxidized methionine (Met-SO) residues, methionine sulfoxide reductases (Msrs) play important role in survival and virulence of Salmonella Typhimurium (S. Typhimurium). Salmonella encodes five msrs. Through the generation of single and cumulative deletion mutants (ΔmsrA, ΔmsrP, ΔmsrAC, ΔmsrACP, ΔmsrACPB, and ΔmsrACPBbisC), we analyzed the relative contribution of various msr genes (msrA, msrB, msrC, msrP, and bisC) in oxidative stress survival of S. Typhimurium. We evaluated the effects of msr gene deletion(s) on protein oxidation, survival in immune cells, colonization in poultry organs, and immune responses. The mutant strains exhibited elevated levels of protein aggregation, with the ∆msrACPBbisC strain accumulating the highest levels of protein aggregates. Survival assays in macrophages and dendritic cells demonstrated that the msrA, msrC, and bisC genes play critical roles in proliferation in immune cells, whereas the contribution of msrP is minimal. Mutants are defective in cecal colonization and systemic dissemination to the spleen and liver, the degree of which depends on the number of mutations. One-day-old female White Leghorn chicks were inoculated with msr mutant strains showed modulated humoral as well as cellular immune responses as compared to S. Typhimurium infected counterpart. These findings underscore the critical roles of msr genes in colonization in poultry and modulation of immune responses, and have implications in the design and development of live vaccines against S. Typhimurium for poultry.