Signal transduction and phosphoryl transfer by a FixL hybrid kinase with low oxygen affinity: importance of the vicinal PAS domain and receiver aspartate

Biochemistry. 2013 Jan 22;52(3):456-65. doi: 10.1021/bi300991r. Epub 2013 Jan 7.

Abstract

FixL is a prototype for heme-based sensors, multidomain proteins that typically couple a histidine protein kinase activity to a heme-binding domain for sensing of diatomic gases such as oxygen, carbon monoxide, and nitric oxide. Despite the relatively well-developed understanding of FixL, the importance of some of its domains has been unclear. To explore the impact of domain-domain interactions on oxygen sensing and signal transduction, we characterized and investigated Rhizobium etli hybrid sensor ReFixL. In ReFixL, the core heme-containing PAS domain and kinase region is preceded by an N-terminal PAS domain of unknown function and followed by a C-terminal receiver domain. The latter resembles a target substrate domain that usually occurs independently of the kinase and contains a phosphorylatable aspartate residue. We isolated the full-length ReFixL as a soluble holoprotein with a single heme b cofactor. Despite a low affinity for oxygen (K(d) for O₂ of 738 μM), the kinase activity was completely switched off by O₂ at concentrations well below the K(d). A deletion of the first PAS domain strongly increased the oxygen affinity but essentially prohibited autophosphorylation, although the truncated protein was competent to accept phosphoryl groups in trans. These studies provide new insights into histidyl-aspartyl phosphoryl transfers in two-component systems and suggest that the control of ligand affinity and signal transduction by PAS domains can be direct or indirect.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Substitution
  • Aspartic Acid / metabolism*
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Heme / metabolism
  • Hemeproteins / chemistry
  • Hemeproteins / genetics
  • Hemeproteins / metabolism*
  • Histidine / metabolism
  • Histidine Kinase
  • Kinetics
  • Ligands
  • Mutant Proteins / chemistry
  • Mutant Proteins / metabolism
  • Oxidation-Reduction
  • Oxygen / metabolism*
  • Peptide Fragments / chemistry
  • Peptide Fragments / genetics
  • Peptide Fragments / metabolism
  • Phosphorylation
  • Protein Binding
  • Protein Interaction Domains and Motifs
  • Protein Processing, Post-Translational
  • Protein Serine-Threonine Kinases / chemistry
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism*
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • Rhizobium / enzymology
  • Rhizobium / metabolism
  • Signal Transduction*

Substances

  • Bacterial Proteins
  • Hemeproteins
  • Ligands
  • Mutant Proteins
  • Peptide Fragments
  • Recombinant Proteins
  • Aspartic Acid
  • Heme
  • Histidine
  • PAS domain kinases
  • Protein Serine-Threonine Kinases
  • FixL protein, Bacteria
  • Histidine Kinase
  • Oxygen