Conserved structural features anchor biofilm‐associated RTX–adhesins to the outer membrane of bacteria. (6th April 2018)

• Record Type: Journal Article
• Authors: Guo, Shuaiqi; Langelaan, David N.; Phippen, Sean W.; Smith, Steven P.; Voets, Ilja K.; Davies, Peter L.
• Is Part Of: FEBS journal. Volume 285:Number 10(2018)
• Page Start: 1812
• Page End: 1826
• Publication Date: 2018-04-06
• Subjects: bacterial adhesins -- biofilms -- structural biology -- surface‐retention domains; Biochemistry -- Periodicals; Molecular biology -- Periodicals; Pathology, Molecular -- Periodicals; 572
• DOI: 10.1111/febs.14441
• Languages: English
• ISSNs: 1742-464X

Abstract

Abstract : Repeats‐in‐toxin (RTX) adhesins are present in many Gram‐negative bacteria to facilitate biofilm formation. Previously, we reported that the 1.5‐MDa RTX adhesin ( Mp IBP) from the Antarctic bacterium, Marinomonas primoryensis, is tethered to the bacterial cell surface via its N‐terminal Region I (RI). Here, we show the detailed structural features of RI. It has an N‐terminal periplasmic retention domain (RIN), a central domain (RIM) that can insert into the β‐barrel of an outer‐membrane pore protein during Mp IBP secretion, and three extracellular domains at its C terminus (RIC) that transition the protein into the extender region (RII). RIN has a novel β‐sandwich fold with a similar shape to βγ‐crystallins and tryptophan RNA attenuation proteins. Because RIM undergoes fast and extensive degradation in vitro, its narrow cylindrical shape was rapidly measured by small‐angle X‐ray scattering before proteolysis could occur. The crystal structure of RIC comprises three tandem β‐sandwich domains similar to those in RII, but increasing in their hydrophobicity with proximity to the outer membrane. In addition, the key Ca 2+ ion that rigidifies the linkers between RII domains is not present between the first two of these RIC domains. This more flexible RI linker near the cell surface can act as a 'pivot' to help the 0.6‐μm‐long Mp IBP sweep over larger volumes to find its binding partners. Since the physical features of RI are well conserved in the RTX adhesins of many Gram‐negative bacteria, our detailed structural and bioinformatic analyses serve as a model for investigating the surface retention of biofilm‐forming bacteria, including human pathogens. Abstract : Proposed mechanism of the cell‐surface retention of RTX adhesins, and the assembly/disassembly processes of the Type I Secretion System (T1SS) channel: upon contact with the C terminus of Mp IBP, the T1SS translocase complex recruits an outer membrane to form a continuous channel across the cell envelope. After Mp IBP plugs TolC with its N‐terminal modules, the T1SS channel will disassemble.