Structure and Properties of a Non-processive, Salt-requiring, and Acidophilic Pectin Methylesterase from Aspergillus niger Provide Insights into the Key Determinants of Processivity Control

J Biol Chem. 2016 Jan 15;291(3):1289-306. doi: 10.1074/jbc.M115.673152. Epub 2015 Nov 14.

Abstract

Many pectin methylesterases (PMEs) are expressed in plants to modify plant cell-wall pectins for various physiological roles. These pectins are also attacked by PMEs from phytopathogens and phytophagous insects. The de-methylesterification by PMEs of the O6-methyl ester groups of the homogalacturonan component of pectin, exposing galacturonic acids, can occur processively or non-processively, respectively, describing sequential versus single de-methylesterification events occurring before enzyme-substrate dissociation. The high resolution x-ray structures of a PME from Aspergillus niger in deglycosylated and Asn-linked N-acetylglucosamine-stub forms reveal a 10⅔-turn parallel β-helix (similar to but with less extensive loops than bacterial, plant, and insect PMEs). Capillary electrophoresis shows that this PME is non-processive, halophilic, and acidophilic. Molecular dynamics simulations and electrostatic potential calculations reveal very different behavior and properties compared with processive PMEs. Specifically, uncorrelated rotations are observed about the glycosidic bonds of a partially de-methyl-esterified decasaccharide model substrate, in sharp contrast to the correlated rotations of processive PMEs, and the substrate-binding groove is negatively not positively charged.

Keywords: capillary electrophoresis; carbohydrate processing; crystal structure; electrostatics; molecular dynamics; pectin methylesterase; processivity.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Amino Acid Substitution
  • Aspergillus niger / enzymology*
  • Carboxylic Ester Hydrolases / chemistry*
  • Carboxylic Ester Hydrolases / genetics
  • Carboxylic Ester Hydrolases / metabolism
  • Catalytic Domain
  • Consensus Sequence
  • Fungal Proteins / chemistry*
  • Fungal Proteins / genetics
  • Fungal Proteins / metabolism
  • Hydrogen-Ion Concentration
  • Models, Molecular*
  • Molecular Dynamics Simulation
  • Molecular Sequence Data
  • Mutation
  • Osmolar Concentration
  • Peptide Fragments / chemistry
  • Peptide Fragments / genetics
  • Peptide Fragments / metabolism
  • Protein Conformation
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • Sequence Alignment
  • Structural Homology, Protein
  • Substrate Specificity
  • X-Ray Diffraction

Substances

  • Fungal Proteins
  • Peptide Fragments
  • Recombinant Proteins
  • Carboxylic Ester Hydrolases
  • pectinesterase

Associated data

  • PDB/1gq8
  • PDB/1qjv
  • PDB/1xg2
  • PDB/2PQR
  • PDB/2nsp
  • PDB/2nt6
  • PDB/2nt9
  • PDB/2ntp
  • PDB/4pmh
  • PDB/5c1c
  • PDB/5c1e