Structures of the Ultra-High-Affinity Protein-Protein Complexes of Pyocins S2 and AP41 and Their Cognate Immunity Proteins from Pseudomonas aeruginosa

J Mol Biol. 2015 Aug 28;427(17):2852-66. doi: 10.1016/j.jmb.2015.07.014. Epub 2015 Jul 26.

Abstract

How ultra-high-affinity protein-protein interactions retain high specificity is still poorly understood. The interaction between colicin DNase domains and their inhibitory immunity (Im) proteins is an ultra-high-affinity interaction that is essential for the neutralisation of endogenous DNase catalytic activity and for protection against exogenous DNase bacteriocins. The colicin DNase-Im interaction is a model system for the study of high-affinity protein-protein interactions. However, despite the fact that closely related colicin-like bacteriocins are widely produced by Gram-negative bacteria, this interaction has only been studied using colicins from Escherichia coli. In this work, we present the first crystal structures of two pyocin DNase-Im complexes from Pseudomonas aeruginosa, pyocin S2 DNase-ImS2 and pyocin AP41 DNase-ImAP41. These structures represent divergent DNase-Im subfamilies and are important in extending our understanding of protein-protein interactions for this important class of high-affinity protein complex. A key finding of this work is that mutations within the immunity protein binding energy hotspot, helix III, are tolerated by complementary substitutions at the DNase-Immunity protein binding interface. Im helix III is strictly conserved in colicins where an Asp forms polar interactions with the DNase backbone. ImAP41 contains an Asp-to-Gly substitution in helix III and our structures show the role of a co-evolved substitution where Pro in DNase loop 4 occupies the volume vacated and removes the unfulfilled hydrogen bond. We observe the co-evolved mutations in other DNase-Immunity pairs that appear to underpin the split of this family into two distinct groups.

Keywords: P aeruginosa.; bacteriocin; immunity protein; pyocin AP41; pyocin S2.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Base Sequence
  • Colicins / metabolism
  • Crystallography, X-Ray
  • Deoxyribonucleases / metabolism
  • Deoxyribonucleases / ultrastructure
  • Molecular Sequence Data
  • Multiprotein Complexes / genetics
  • Multiprotein Complexes / metabolism
  • Multiprotein Complexes / ultrastructure*
  • Mutation
  • Phylogeny
  • Protein Binding
  • Protein Interaction Mapping
  • Protein Structure, Tertiary / genetics
  • Pseudomonas aeruginosa / genetics
  • Pseudomonas aeruginosa / metabolism*
  • Pyocins / metabolism*
  • Sequence Analysis, DNA

Substances

  • Colicins
  • Multiprotein Complexes
  • Pyocins
  • pyocin AP41
  • Deoxyribonucleases

Associated data

  • PDB/4QKO
  • PDB/4UHP
  • PDB/4UHQ