Expansion of Auxiliary Activity Family 5 sequence space via biochemical characterization of six new copper radical oxidases

Appl Environ Microbiol. 2024 Jul 24;90(7):e0101424. doi: 10.1128/aem.01014-24. Epub 2024 Jul 2.

Abstract

Bacterial and fungal copper radical oxidases (CROs) from Auxiliary Activity Family 5 (AA5) are implicated in morphogenesis and pathogenesis. The unique catalytic properties of CROs also make these enzymes attractive biocatalysts for the transformation of small molecules and biopolymers. Despite a recent increase in the number of characterized AA5 members, especially from subfamily 2 (AA5_2), the catalytic diversity of the family as a whole remains underexplored. In the present study, phylogenetic analysis guided the selection of six AA5_2 members from diverse fungi for recombinant expression in Komagataella pfaffii (syn. Pichia pastoris) and biochemical characterization in vitro. Five of the targets displayed predominant galactose 6-oxidase activity (EC 1.1.3.9), and one was a broad-specificity aryl alcohol oxidase (EC 1.1.3.7) with maximum activity on the platform chemical 5-hydroxymethyl furfural (EC 1.1.3.47). Sequence alignment comparing previously characterized AA5_2 members to those from this study indicated various amino acid substitutions at active site positions implicated in the modulation of specificity.IMPORTANCEEnzyme discovery and characterization underpin advances in microbial biology and the application of biocatalysts in industrial processes. On one hand, oxidative processes are central to fungal saprotrophy and pathogenesis. On the other hand, controlled oxidation of small molecules and (bio)polymers valorizes these compounds and introduces versatile functional groups for further modification. The biochemical characterization of six new copper radical oxidases further illuminates the catalytic diversity of these enzymes, which will inform future biological studies and biotechnological applications.

Keywords: Auxiliary Activity Family 5; HMF oxidase; alcohol oxidase; carbohydrate-active enzyme; copper radical oxidase; galactose oxidase.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alcohol Oxidoreductases / chemistry
  • Alcohol Oxidoreductases / genetics
  • Alcohol Oxidoreductases / metabolism
  • Amino Acid Sequence
  • Catalytic Domain
  • Copper* / metabolism
  • Fungal Proteins / chemistry
  • Fungal Proteins / genetics
  • Fungal Proteins / metabolism
  • Galactose Oxidase / chemistry
  • Galactose Oxidase / genetics
  • Galactose Oxidase / metabolism
  • Oxidoreductases* / chemistry
  • Oxidoreductases* / genetics
  • Oxidoreductases* / metabolism
  • Phylogeny*
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Saccharomycetales / enzymology
  • Saccharomycetales / genetics
  • Sequence Alignment
  • Substrate Specificity

Substances

  • Oxidoreductases
  • Copper
  • Fungal Proteins
  • Alcohol Oxidoreductases
  • aryl-alcohol oxidase
  • copper oxidase
  • Galactose Oxidase
  • Recombinant Proteins

Supplementary concepts

  • Komagataella pastoris