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- Title
Architecture of the biofilm-associated archaic Chaperone-Usher pilus CupE from Pseudomonas aeruginosa.
- Authors
Böhning, Jan; Dobbelstein, Adrian W.; Sulkowski, Nina; Eilers, Kira; von Kügelgen, Andriko; Tarafder, Abul K.; Peak-Chew, Sew-Yeu; Skehel, Mark; Alva, Vikram; Filloux, Alain; Bharat, Tanmay A. M.
- Abstract
Chaperone-Usher Pathway (CUP) pili are major adhesins in Gram-negative bacteria, mediating bacterial adherence to biotic and abiotic surfaces. While classical CUP pili have been extensively characterized, little is known about so-called archaic CUP pili, which are phylogenetically widespread and promote biofilm formation by several human pathogens. In this study, we present the electron cryomicroscopy structure of the archaic CupE pilus from the opportunistic human pathogen Pseudomonas aeruginosa. We show that CupE1 subunits within the pilus are arranged in a zigzag architecture, containing an N-terminal donor β-strand extending from each subunit into the next, where it is anchored by hydrophobic interactions, with comparatively weaker interactions at the rest of the inter-subunit interface. Imaging CupE pili on the surface of P. aeruginosa cells using electron cryotomography shows that CupE pili adopt variable curvatures in response to their environment, which might facilitate their role in promoting cellular attachment. Finally, bioinformatic analysis shows the widespread abundance of cupE genes in isolates of P. aeruginosa and the co-occurrence of cupE with other cup clusters, suggesting interdependence of cup pili in regulating bacterial adherence within biofilms. Taken together, our study provides insights into the architecture of archaic CUP pili, providing a structural basis for understanding their role in promoting cellular adhesion and biofilm formation in P. aeruginosa. Author summary: Many bacteria adhere to surfaces or host cells using filamentous structures termed pili that extend from the bacterial cell and anchor them to their target. Previous studies have characterised various Chaperone-Usher Pathway (CUP) pili, which are common in Gram-negative bacteria. However, little is known about the so-called archaic CUP pili, which are the most widespread type. Archaic CUP pili help maintain the architecture of multicellular bacterial aggregates termed biofilms formed by the pathogen Pseudomonas aeruginosa and many others. In this study, we present a cryo-EM structure of the archaic CUP pilus CupE from P. aeruginosa, providing a structural basis of how the CupE1 protein forms zigzag-shaped, extended pili. By imaging CupE pili on P. aeruginosa cells using electron cryotomography, we show that pili can adopt variable long-range curvature, which may help their role in providing cohesion between cells within the biofilm. Furthermore, structural modelling provides insights into the roles of minor pilin subunits encoded within the cupE operon. These results will help advance our understanding of bacterial pili structure and function.
- Subjects
QUORUM sensing; ELECTRON cryomicroscopy; PSEUDOMONAS aeruginosa; HYDROPHOBIC interactions; GRAM-negative bacteria; BACTERIAL cells; STRUCTURAL models
- Publication
PLoS Pathogens, 2023, Vol 18, Issue 4, p1
- ISSN
1553-7366
- Publication type
Article
- DOI
10.1371/journal.ppat.1011177