A glyoxal-specific aldehyde signaling axis in Pseudomonas aeruginosa that influences quorum sensing and infection

Christopher J. Corcoran, Bonnie J. Cuthbert, David G. Glanville, Mailyn Terrado, Diana Valverde Mendez, Benjamin P. Bratton, Daniel E. Schemenauer, Valerie L. Tokars, Thomas G. Martin, Lawrence W. Rasmussen, Matthew C. Madison, Andrew F. Maule, Joshua W. Shaevitz, Boo Shan Tseng, Julian P. Whitelegge, Catherine Putonti, Amit Gaggar, Jordan R. Beach, Jonathan A. Kirk, Alfonso Mondragón, Abby R. Kroken, Jonathan P. Allen, Celia W. Goulding and Andrew T. Ulijasz ()
Additional contact information
Christopher J. Corcoran: Loyola University Chicago
Bonnie J. Cuthbert: Irvine
David G. Glanville: University of Alabama at Birmingham
Mailyn Terrado: Loyola University Chicago
Diana Valverde Mendez: Princeton University
Benjamin P. Bratton: Vanderbilt University Medical Center
Daniel E. Schemenauer: Loyola University Chicago
Valerie L. Tokars: Northwestern University
Thomas G. Martin: Loyola University Chicago Stritch School of Medicine
Lawrence W. Rasmussen: University of Alabama at Birmingham
Matthew C. Madison: University of Alabama at Birmingham
Andrew F. Maule: University of Wisconsin-Madison
Joshua W. Shaevitz: Princeton University
Boo Shan Tseng: University of Nevada Las Vegas
Julian P. Whitelegge: Los Angeles
Catherine Putonti: Loyola University Chicago
Amit Gaggar: University of Alabama at Birmingham
Jordan R. Beach: Loyola University Chicago Stritch School of Medicine
Jonathan A. Kirk: Loyola University Chicago Stritch School of Medicine
Alfonso Mondragón: Northwestern University
Abby R. Kroken: Loyola University Chicago
Jonathan P. Allen: Loyola University Chicago
Celia W. Goulding: University of California Irvine
Andrew T. Ulijasz: University of Alabama at Birmingham

Nature Communications, 2025, vol. 16, issue 1, 1-24

Abstract: Abstract The universally conserved α-oxoaldehydes glyoxal (GO) and methylglyoxal (MGO) are toxic metabolic byproducts whose accumulation can lead to cell death. In the absence of a known, natural inducer of the GO-specific response in prokaryotes, we exploited RNA-seq to define a GO response in the bacterial pathogen Pseudomonas aeruginosa. The highest upregulated operon consisted of the known glyoxalase (gloA2) and an antibiotic monooxygenase (ABM) domain of unknown function - renamed here Aldehyde responsive quorum-sensing Inhibitor (ArqI). The arqI-gloA2 operon is highly specific to GO induction and ArqI protein responds by migrating to the flagellar pole. An ArqI atomic structure revealed several unique features to the ABM family, including a ‘pinwheel’ hexamer harboring a GO-derived post-translational modification on a conserved arginine residue (Arg49). Induction of ArqI abrogates production of the Pseudomonas Quinolone Signal (PQS) quorum sensing molecule and was found to directly interact with PqsA; the first enzyme in the PQS biosynthesis pathway. Finally, we use a sepsis model of infection to reveal a survival requirement for arqI-gloA2 in blood-rich organs (heart, spleen, liver and lung). Here we define a global GO response in a pathogen, identify and characterize the first GO-specific operon and implicate its role in PQS production and host survival.

Date: 2025
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DOI: 10.1038/s41467-025-61469-8

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