Structural dynamics of RbmA governs plasticity of Vibrio cholerae biofilms.

Jiunn Cn Fong,Andrew Rogers,Raimo Hartmann,Carrie L Partch,Praveen K Singh,Fitnat H Yildiz,Lars Ep Dietrich,Yu-Cheng Lin,Alicia K Michael,Nicole C Parsley,Knut Drescher,Evgeny Vinogradov,William-Cole Cornell

doi:10.7554/elife.26163

Abstract

Biofilm formation is critical for the infection cycle of Vibrio cholerae. Vibrio exopolysaccharides (VPS) and the matrix proteins RbmA, Bap1 and RbmC are required for the development of biofilm architecture. We demonstrate that RbmA binds VPS directly and uses a binary structural switch within its first fibronectin type III (FnIII-1) domain to control RbmA structural dynamics and the formation of VPS-dependent higher-order structures. The structural switch in FnIII-1 regulates interactions in trans with the FnIII-2 domain, leading to open (monomeric) or closed (dimeric) interfaces. The ability of RbmA to switch between open and closed states is important for V. cholerae biofilm formation, as RbmA variants with switches that are locked in either of the two states lead to biofilms with altered architecture and structural integrity.

Highlights

In nature, microorganisms are predominantly found in biofilms, embedded within a matrix composed of exopolysaccharides, proteins, lipids and nucleic acids
Structural analysis of RbmA revealed that two tandem fibronectin type III (FnIII) domains (FnIII-1 and FnIII-2), which are connected by a short linker and interact in trans in an antiparallel orientation to form a stable dimer (Giglio et al, 2013; Maestre-Reyna et al, 2013)
In the O-loop conformation, the c strand of the FnIII-1 domain is largely unfolded to facilitate a network of interactions between b residue D97 and the FnIII-1 and FnIII-2 domains to stabilize the closed dimer interface, whereas these interactions are abolished in the D-loop conformation (Figure 1B and Figure 1—figure supplement 1)

Summary

Introduction

Microorganisms are predominantly found in biofilms, embedded within a matrix composed of exopolysaccharides, proteins, lipids and nucleic acids. The ability to form biofilms enhances growth and survival of the pathogen outside the body of its mammalian host by providing protection from a number of environmental stresses, including nutrient limitation and predation by protozoa and bacteriophages (Yildiz and Schoolnik, 1999; Matz et al, 2005; Beyhan and Yildiz, 2007). Production of biofilms by V. cholerae requires extracellular matrix components, such as the Vibrio exopolysaccharide (VPS) and the matrix proteins RbmA, RbmC, and Bap (Yildiz and Schoolnik, 1999; Fong et al, 2006; Fong and Yildiz, 2007; Fong et al, 2010; Absalon et al, 2011; Berk et al, 2012). RbmA controls the arrangements of V. cholerae cells relative to the substratum during biofilm development, and in turn, governs development of mature biofilm architecture (Drescher et al, 2016)

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Conclusion