Firmicutes and dermatophytes degrade recalcitrant insoluble keratins resistant to proteolysis. Such highly ordered peptide fibrils can be digested through proteolysis as well as sulfitolysis. However, its biological mechanism relevant to keratin degradation remains unclear. Here we present genome-wide multi-omics analyses to describe how the extremophilic bacterium Fervidobacterium islandicum AW-1degrades keratin under stress conditions. Physiological and biochemical evidence integrated with multi-omics data reveals a nutrient deprivation-induced metabolic shift, thereby increasing chemotactic persister formation for cellular adhesion to keratins and activating the membrane-associated keratinolysis. Quantitative dynamic gene expression and metabolite profiling confirmed that stringent response-induced flagella synthesis is a prerequisite for biofilm formation and that keratin degradation is responsible for swarming dispersal. This study illustrates the molecular details of keratinolysis, providing insight into the survivability of primordial bacteria coping with scarce nutrition relevant to recurrent infections with superficial pathogens.