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

FEBS J. 2018 Apr;285(8):1511-1527. doi: 10.1111/febs.14424. Epub 2018 Mar 13.

Abstract

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).

Keywords: Shewanella frigidimarina; Antarctic bacteria; adhesion; antifreeze; ice-binding protein.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adhesins, Bacterial / chemistry
  • Adhesins, Bacterial / genetics
  • Adhesins, Bacterial / metabolism*
  • Amino Acid Sequence
  • Antarctic Regions
  • Bacterial Adhesion
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Crystallography, X-Ray
  • Ice*
  • Models, Molecular
  • Protein Domains
  • Sequence Homology, Amino Acid
  • Shewanella / genetics
  • Shewanella / metabolism*

Substances

  • Adhesins, Bacterial
  • Bacterial Proteins
  • Ice

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