<i> <i>Vibrio cholerae</i> </i> biofilm matrix assembly and growth are shaped by a glutamate-specific TAXI/TRAP protein

Biofilms are critical for the environmental persistence, survival, and infectivity of <i><i>Vibrio cholerae</i></i>, the causative agent of cholera. Here, we find that GluP, a glutamate-specific TRAP-TAXI protein, is an uncharacterized matrix component that plays a critical role in biofilm architecture. Loss of GluP reduces biofilm corrugation, expands colony size, and disperses cells from microcolonies, arguing that this factor maintains biofilm structure and organization. While GluP does not affect the abundance or localization of known matrix proteins, its absence reduces <i><i>Vibrio</i></i> exopolysaccharide (VPS) production. We determined the crystal structure of GluP, which revealed that GluP binds glutamate, and its biofilm-related phenotypes depend on this binding capability. We further examined the role of GluP in <i>V. cholerae</i> growth under defined conditions where L-glutamate serves as a carbon source, nitrogen source, or both. GluP-deficient strains specifically showed reduced growth when glucose was the carbon source and glutamate the nitrogen source. This defect is dependent on glutamate binding by GluP and highlights its role in coordinating nutrient acquisition and biofilm formation. Importantly, both biofilm assembly and growth defects occurred independently of the predicted membrane component of the Glu TRAP-TAXI system, GluQM. These findings indicate that GluP plays a dual role in biofilm assembly and growth, providing insight into its functional importance in <i>V. cholerae</i> physiology.

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Publication Details

Journal
Proceedings of the National Academy of Sciences
Published
2025-12-09
DOI
https://doi.org/10.1073/pnas.2504869122
Primary Topic
Bacterial biofilms and quorum sensing
Type
article
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article

Vibrio cholerae biofilm matrix assembly and growth are shaped by a glutamate-specific TAXI/TRAP protein

Ethan A. Older, Evgeny Vinogradov, Kaitlin D Yarrington, Kyle A. Floyd et al.
Proceedings of the National Academy of Sciences
Bacterial biofilms and quorum sensing
article

Vibrio cholerae biofilm matrix assembly and growth are shaped by a glutamate-specific TAXI/TRAP protein

Ethan A. Older, Evgeny Vinogradov, Kaitlin D Yarrington, Kyle A. Floyd, Peter J. Yunker, James B. Winans, Anna Potapova, Fitnat H. Yildiz, Christopher R. Evans, Dominique H. Limoli, Laura M. Sanchez, Holger Sondermann, Carey D. Nadell, W. Timothy Garvey, Sofia Piepoli, Lars E. P. Dietrich, Miles T. Wetherington, Steffi Jimmy, Olivia F Schakel, Rino Oguchi
article en

Abstract

Biofilms are critical for the environmental persistence, survival, and infectivity of <i><i>Vibrio cholerae</i></i>, the causative agent of cholera. Here, we find that GluP, a glutamate-specific TRAP-TAXI protein, is an uncharacterized matrix component that plays a critical role in biofilm architecture. Loss of GluP reduces biofilm corrugation, expands colony size, and disperses cells from microcolonies, arguing that this factor maintains biofilm structure and organization. While GluP does not affect the abundance or localization of known matrix proteins, its absence reduces <i><i>Vibrio</i></i> exopolysaccharide (VPS) production. We determined the crystal structure of GluP, which revealed that GluP binds glutamate, and its biofilm-related phenotypes depend on this binding capability. We further examined the role of GluP in <i>V. cholerae</i> growth under defined conditions where L-glutamate serves as a carbon source, nitrogen source, or both. GluP-deficient strains specifically showed reduced growth when glucose was the carbon source and glutamate the nitrogen source. This defect is dependent on glutamate binding by GluP and highlights its role in coordinating nutrient acquisition and biofilm formation. Importantly, both biofilm assembly and growth defects occurred independently of the predicted membrane component of the Glu TRAP-TAXI system, GluQM. These findings indicate that GluP plays a dual role in biofilm assembly and growth, providing insight into its functional importance in <i>V. cholerae</i> physiology.

Proceedings of the National Academy of SciencesVol. 122(50)
Dartmouth College (US), University of Iowa (US), Georgia Institute of Technology (US), University of California, Santa Cruz (US), Deutsches Elektronen-Synchrotron DESY (DE), Christian-Albrechts-Universität zu Kiel (DE), Indiana University Bloomington (US), National Research Council Canada (CA), Indiana University (US), Columbia University (US)
Openalex Percentile: Top 64%
Bacterial biofilms and quorum sensing
DOIOpen Access PDFOpenAlex
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