The GlnD and GlnK homologues of Streptomyces coelicolor A3(2) are functionally dissimilar to their nitrogen regulatory system counterparts from enteric bacteria

Mol Microbiol. 2002 Oct;46(2):319-30. doi: 10.1046/j.1365-2958.2002.03149.x.

Abstract

Glutamine synthetase I (GSI) enzyme activity in Streptomyces coelicolor is controlled post-translationally by the adenylyltransferase (GlnE) as in enteric bacteria. Although other homologues of the Escherichia coli Ntr system (glnK, coding for a PII family protein; and glnD, coding for an uridylyltransferase) are found in the S. coelicolor genome, the regulation of the GSI activity was found to be different. The functions of glnK and glnD were analysed by specific mutants. Surprisingly, biochemical assay and two-dimensional PAGE analysis showed that modification of GSI by GlnE occurs normally in all mutant strains, and neither GlnK nor GlnD are required for the regulation of GlnE in response to nitrogen stimuli. Analysis of the post-translational regulation of GlnK in vivo by two-dimensional PAGE and mass spectrometry indicated that it is subject to both a reversible and a non-reversible modification in a direct response to nitrogen availability. The irreversible modification was identified as removal of the first three N-terminal amino acid residues of the protein, and the reversible modification as adenylylation of the conserved tyro-sine 51 residue that is known to be uridylylated in E. coli. The glnD insertion mutant expressing only the N-terminal half of GlnD was capable of adenylylating GlnK, but was unable to perform the reverse deadenylylation reaction in response to excess ammonium. The glnD null mutant completely lacked the ability to adenylylate GlnK. This work provides the first example of a PII protein that is modified by adenylylation, and demonstrates that this reaction is performed by a homologue of GlnD, previously described only as a uridylyltransferase enzyme.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Bacterial Proteins*
  • Carrier Proteins / chemistry
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • DNA, Bacterial / analysis
  • Electrophoresis, Gel, Two-Dimensional
  • Escherichia coli / enzymology*
  • Escherichia coli / genetics
  • Gene Expression Regulation, Bacterial
  • Glutamate-Ammonia Ligase / metabolism
  • Molecular Sequence Data
  • Mutation
  • Nitrogen / metabolism
  • Nucleotidyltransferases / chemistry
  • Nucleotidyltransferases / genetics
  • Nucleotidyltransferases / metabolism*
  • PII Nitrogen Regulatory Proteins
  • Sequence Alignment
  • Sequence Homology, Amino Acid
  • Signal Transduction
  • Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization
  • Streptomyces / enzymology*
  • Streptomyces / genetics

Substances

  • Bacterial Proteins
  • Carrier Proteins
  • DNA, Bacterial
  • GlnK protein, Azorhizobium caulinodans
  • PII Nitrogen Regulatory Proteins
  • Nucleotidyltransferases
  • regulatory protein uridylyltransferase
  • Glutamate-Ammonia Ligase
  • Nitrogen