A Pseudomonas aeruginosa small RNA regulates chronic and acute infection

Pengbo Cao, Derek Fleming, Dina A. Moustafa, Stephen K. Dolan, Kayla H. Szymanik, Whitni K. Redman, Anayancy Ramos, Frances L. Diggle, Christopher S. Sullivan, Joanna B. Goldberg, Kendra P. Rumbaugh and Marvin Whiteley ()
Additional contact information
Pengbo Cao: School of Biological Sciences, Georgia Institute of Technology
Derek Fleming: Texas Tech University Health Sciences Center
Dina A. Moustafa: Emory-Children’s Cystic Fibrosis Center
Stephen K. Dolan: School of Biological Sciences, Georgia Institute of Technology
Kayla H. Szymanik: The University of Texas at Austin
Whitni K. Redman: Texas Tech University Health Sciences Center
Anayancy Ramos: School of Biological Sciences, Georgia Institute of Technology
Frances L. Diggle: School of Biological Sciences, Georgia Institute of Technology
Christopher S. Sullivan: The University of Texas at Austin
Joanna B. Goldberg: Emory-Children’s Cystic Fibrosis Center
Kendra P. Rumbaugh: Texas Tech University Health Sciences Center
Marvin Whiteley: School of Biological Sciences, Georgia Institute of Technology

Nature, 2023, vol. 618, issue 7964, 358-364

Abstract: Abstract The ability to switch between different lifestyles allows bacterial pathogens to thrive in diverse ecological niches1,2. However, a molecular understanding of their lifestyle changes within the human host is lacking. Here, by directly examining bacterial gene expression in human-derived samples, we discover a gene that orchestrates the transition between chronic and acute infection in the opportunistic pathogen Pseudomonas aeruginosa. The expression level of this gene, here named sicX, is the highest of the P. aeruginosa genes expressed in human chronic wound and cystic fibrosis infections, but it is expressed at extremely low levels during standard laboratory growth. We show that sicX encodes a small RNA that is strongly induced by low-oxygen conditions and post-transcriptionally regulates anaerobic ubiquinone biosynthesis. Deletion of sicX causes P. aeruginosa to switch from a chronic to an acute lifestyle in multiple mammalian models of infection. Notably, sicX is also a biomarker for this chronic-to-acute transition, as it is the most downregulated gene when a chronic infection is dispersed to cause acute septicaemia. This work solves a decades-old question regarding the molecular basis underlying the chronic-to-acute switch in P. aeruginosa and suggests oxygen as a primary environmental driver of acute lethality.

Date: 2023
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DOI: 10.1038/s41586-023-06111-7

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