An ice‐binding and tandem beta‐sandwich domain‐containing protein in Shewanella frigidimarina is a potential new type of ice adhesin

• Published in: The FEBS journal Vol. 285; no. 8; pp. 1511 - 1527
• Main Authors: Vance, Tyler D.R., Graham, Laurie A., Davies, Peter L.
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01.04.2018
• Subjects: Adhesins, Bacterial - chemistry; Adhesins, Bacterial - genetics; Adhesins, Bacterial - metabolism; adhesion; Amino Acid Sequence; Antarctic bacteria; Antarctic Regions; antifreeze; Bacterial Adhesion; Bacterial Proteins - chemistry; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; Crystallography; Crystallography, X-Ray; Data banks; Electrostatic properties; Fluorescence; Gene transfer; Ice; ice‐binding protein; Microorganisms; Models, Molecular; Protein Domains; Protein structure; Proteins; Recrystallization; Sequence Homology, Amino Acid; Shewanella; Shewanella - genetics; Shewanella - metabolism; Shewanella frigidimarina; Antarctic Regions; adhesion; Shewanella frigidimarina; ice-binding protein; Antarctic bacteria; antifreeze
• ISSN: 1742-464X; 1742-4658
• DOI: 10.1111/febs.14424

Out of the dozen different ice‐binding protein (IBP) structures known, the DUF3494 domain is the most widespread, having been passed many times between prokaryotic and eukaryotic microorganisms by horizontal gene transfer. This ~25‐kDa β‐solenoid domain with an adjacent parallel α‐helix is most commonly associated with an N‐terminal secretory signal peptide. However, examples of the DUF3494 domain preceded by tandem Bacterial Immunoglobulin‐like (BIg) domains are sometimes found, though uncharacterized. Here, we present one such protein (SfIBP_1) from the Antarctic bacterium Shewanella frigidimarina. We have confirmed and characterized the ice‐binding activity of its ice‐binding domain using thermal hysteresis measurements, fluorescent ice plane affinity analysis, and ice recrystallization inhibition assays. X‐ray crystallography was used to solve the structure of the SfIBP_1 ice‐binding domain, to further characterize its ice‐binding surface and unique method of stabilizing or ‘capping’ the ends of the solenoid structure. The latter is formed from the interaction of two loops mediated by a combination of tandem prolines and electrostatic interactions. Furthermore, given their domain architecture and membrane association, we propose that these BIg‐containing DUF3494 IBPs serve as ice‐binding adhesion proteins that are capable of adsorbing their host bacterium onto ice. Database Submitted new structure to the Protein Data Bank (PDB: 6BG8). We present the structural and functional characterization of a putative ice‐binding protein (IBP) from the Antarctic bacterium Shewanella frigidimarina. The protein contains an active ice‐binding domain belonging to the widespread DUF3494 protein fold family, which – along with its multidomain architecture and localization to the membrane within the cell – suggests a potential role in adhering its host to ice.