The response to desiccation in <i>Acinetobacter baumannii</i>

The long-term resistance to desiccation on abiotic surfaces is a key determinant of the adaptive success of <i>Acinetobacter baumannii</i> as a healthcare-associated bacterial pathogen. Here, the cellular and molecular mechanisms enabling <i>A. baumannii</i> to resist desiccation and persist on abiotic surfaces were investigated. Experiments were set up to mimic the <i>A. baumannii</i> response to air-drying that would occur when bacterial cells contaminate fomites in hospitals. Resistance to desiccation and transition to the "viable but nonculturable" (VBNC) state were determined in the laboratory-adapted strain ATCC 19606^T and the epidemic strain ACICU. Culturability, membrane integrity, metabolic activity, virulence, and gene expression profile were compared between the two strains at different stages of desiccation. Upon desiccation, ATCC 19606^T and ACICU cells lose culturability and membrane integrity, lower their metabolism, and enter the VBNC state. However, desiccated <i>A. baumannii</i> cells fully recover culturability and virulence in an insect infection model following rehydration in physiological buffers or human biological fluids. Transcriptome and chemical analyses of <i>A. baumannii</i> cells during desiccation unveiled the production of protective metabolites (L-cysteine and L-glutamate) and decreased energetic metabolism consequent to activation of the glyoxylate shunt (GS) pathway, as confirmed by reduced resuscitation efficiency of <i>aceA</i> mutants, lacking the key enzyme of the GS pathway. VBNC cell formation and extensive metabolic reprogramming provide a biological basis for the response of <i>A. baumannii</i> to desiccation, with implications on environmental control measures aimed at preventing the transmission of <i>A. baumannii</i> infection in hospitals.