Conserved residues in Ycf54 are required for protochlorophyllide formation in Synechocystis sp. PCC 6803

Biochem J. 2017 Feb 20;474(5):667-681. doi: 10.1042/BCJ20161002.

Abstract

Chlorophylls (Chls) are modified tetrapyrrole molecules, essential for photosynthesis. These pigments possess an isocyclic E ring formed by the Mg-protoporphyrin IX monomethylester cyclase (MgPME-cyclase). We assessed the in vivo effects of altering seven highly conserved residues within Ycf54, which is required for MgPME-cyclase activity in the cyanobacterium SynechocystisSynechocystis strains harbouring the Ycf54 alterations D39A, F40A and R82A were blocked to varying degrees at the MgPME-cyclase step, whereas the A9G mutation reduced Ycf54 levels by ∼75%. Wild-type (WT) levels of the cyclase subunit CycI are present in strains with D39A and F40A, but these strains have lowered cellular Chl and photosystem accumulation. CycI is reduced by ∼50% in A9G and R82A, but A9G has no perturbations in Chl or photosystem accumulation, whilst R82A contains very little Chl and few photosystems. When FLAG tagged and used as bait in pulldown experiments, the three mutants D39A, F40A and R82A were unable to interact with the MgPME-cyclase component CycI, whereas A9G pulled down a similar level of CycI as WT Ycf54. These observations suggest that a stable interaction between CycI and Ycf54 is required for unimpeded Pchlide biosynthesis. Crystal structures of the WT, A9G and R82A Ycf54 proteins were solved and analysed to investigate the structural effects of these mutations. A loss of the local hydrogen bonding network and a reversal in the surface charge surrounding residue R82 are probably responsible for the functional differences observed in the R82A mutation. We conclude that the Ycf54 protein must form a stable interaction with CycI to promote optimal Pchlide biosynthesis.

Keywords: Mg-protoporphyrin IX monomethylester cyclase; Ycf54; chlorophyll; oxidative cyclase; photosynthesis; synechocystis.

MeSH terms

  • Amino Acid Sequence
  • Amino Acid Substitution
  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Cloning, Molecular
  • Crystallography, X-Ray
  • Cyclization
  • Escherichia coli / genetics
  • Escherichia coli / metabolism
  • Gene Expression
  • Hydrogen Bonding
  • Mutagenesis, Site-Directed
  • Oxygenases / chemistry*
  • Oxygenases / genetics
  • Oxygenases / metabolism
  • Photosynthesis / genetics
  • Protein Interaction Domains and Motifs
  • Protein Multimerization
  • Protein Structure, Secondary
  • Protein Subunits / chemistry*
  • Protein Subunits / genetics
  • Protein Subunits / metabolism
  • Protochlorophyllide / biosynthesis*
  • Protochlorophyllide / chemistry
  • Protoporphyrins / chemistry
  • Protoporphyrins / metabolism
  • Recombinant Proteins / chemistry*
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Sequence Alignment
  • Sequence Homology, Amino Acid
  • Static Electricity
  • Synechocystis / enzymology
  • Synechocystis / genetics*

Substances

  • Bacterial Proteins
  • Protein Subunits
  • Protoporphyrins
  • Recombinant Proteins
  • magnesium protoporphyrin
  • Protochlorophyllide
  • Oxygenases
  • magnesium protoporphyrin monomethyl ester oxidative cyclase