Structural Study of Metal Binding and Coordination in Ancient Metallo-β-Lactamase PNGM-1 Variants

Int J Mol Sci. 2020 Jul 12;21(14):4926. doi: 10.3390/ijms21144926.

Abstract

The increasing incidence of community- and hospital-acquired infections with multidrug-resistant (MDR) bacteria poses a critical threat to public health and the healthcare system. Although β-lactam antibiotics are effective against most bacterial infections, some bacteria are resistant to β-lactam antibiotics by producing β-lactamases. Among β-lactamases, metallo-β-lactamases (MBLs) are especially worrisome as only a few inhibitors have been developed against them. In MBLs, the metal ions play an important role as they coordinate a catalytic water molecule that hydrolyzes β-lactam rings. We determined the crystal structures of different variants of PNGM-1, an ancient MBL with additional tRNase Z activity. The variants were generated by site-directed mutagenesis targeting metal-coordinating residues. In PNGM-1, both zinc ions are coordinated by six coordination partners in an octahedral geometry, and the zinc-centered octahedrons share a common face. Structures of the PNGM-1 variants confirm that the substitution of a metal-coordinating residue causes the loss of metal binding and β-lactamase activity. Compared with PNGM-1, subclass B3 MBLs lack one metal-coordinating residue, leading to a shift in the metal-coordination geometry from an octahedral to tetrahedral geometry. Our results imply that a subtle change in the metal-binding site of MBLs can markedly change their metal-coordination geometry and catalytic activity.

Keywords: antibiotics; metal coordination; metallo-β-lactamase (MBL); x-ray crystallography.

Publication types

  • Comparative Study

MeSH terms

  • Bacillus subtilis / enzymology
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Binding Sites
  • Catalytic Domain
  • Coordination Complexes / chemistry*
  • Crystallography, X-Ray
  • Drug Resistance, Multiple, Bacterial
  • Endoribonucleases / chemistry*
  • Endoribonucleases / genetics
  • Endoribonucleases / metabolism
  • Evolution, Molecular*
  • Flavobacteriaceae / enzymology
  • Models, Molecular
  • Mutagenesis, Site-Directed
  • Protein Binding
  • Protein Conformation
  • Structure-Activity Relationship
  • Water
  • Zinc* / metabolism
  • beta-Lactamases / chemistry*
  • beta-Lactamases / genetics
  • beta-Lactamases / metabolism

Substances

  • Bacterial Proteins
  • Coordination Complexes
  • Water
  • Endoribonucleases
  • beta-Lactamases
  • Zinc