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Staphylococcus aureus  is a major cause of bovine mastitis, commonly leading to long-lasting, persistent and recurrent infections. Thereby,  S .  aureus  constantly refines and permanently adapts to the bovine udder environment. In this work, we followed  S .  aureus  within-host adaptation over the course of three months in a naturally infected dairy cattle with chronic, subclinical mastitis. Whole genome sequence analysis revealed a complete replacement of the initial predominant variant by another isogenic variant. We report for the first time within-host evolution towards a sigma factor SigB-deficient pathotype in  S .  aureus  bovine mastitis, associated with a single nucleotide polymorphism in  rsbU  (G368A → G122D), a contributor to SigB-functionality. The emerged SigB-deficient pathotype exhibits a substantial shift to new phenotypic traits comprising strong proteolytic activity and poly- N -acetylglucosamine (PNAG)-based biofilm production. This possibly unlocks new nutritional resources and promotes immune evasion, presumably facilitating extracellular persistence within the host. Moreover, we observed an adaptation towards attenuated virulence using a mouse infection model. This study extends the role of sigma factor SigB in  S .  aureus  pathogenesis, so far described to be required for intracellular persistence during chronic infections. Our findings suggest that  S .  aureus  SigB-deficiency is an alternative mechanism for persistence and underpin the clinical relevance of staphylococcal SigB-deficient variants which are consistently isolated during human chronic infections.

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Within-host evolution of bovine Staphylococcus aureus selects for a SigB-deficient pathotype characterized by reduced virulence but enhanced proteolytic activity and biofilm formation