Overall mutational scanning unveils the essential active residues for the mechanistic action of MCR-1

Microbiol Res. 2025 Feb:291:127982. doi: 10.1016/j.micres.2024.127982. Epub 2024 Nov 22.

Abstract

Polymyxins, including colistin and polymyxin B, serve as crucial last-resort antibiotics for managing infections caused by carbapenem-resistant Enterobacterales (CRE). However, the rapid spread of the mobilized colistin resistance gene (mcr-1) challenged the efficacy of treatment by polymyxins. The mcr-1 gene encoded a transmembrane phosphoethanolamine (PEA) transferase enzyme, MCR-1. MCR-1 could catalyze the transfer of PEA moiety of phosphatidylethanolamine (PE) to the 1' (or 4')-phosphate group of the lipid A. Despite the determination of several structures of the soluble domain of MCR-1, the structural and biochemical mechanisms of integral MCR-1 remain less understood. In this study, we utilized an alanine scanning mutagenesis approach to systematically investigate the functional attributes of distinct regions within MCR-1. We identified fifteen critical residues that are indispensable for the enzymatic activity of MCR-1 and are pivotal for its ability to confer resistance to colistin. Furthermore, molecular docking of MCR-1 complexed with the phosphoethanolamine (PE) substrate revealed the presence of a channel-shaped cavity, a characteristic feature shared with other phosphoethanolamine transferases. Despite MCR-1 exhibiting a low sequence identity with both MCR homologues and other phosphoethanolamine (PEA) transferases, several conserved sites were identified, including Y97, M105, K333, H395, L477, and H478, suggesting a potentially shared catalytic mechanism among them for modifying LPS-lipid A. Overall, these findings provide a deep understanding of the catalytic mechanism of MCR-1 for colistin resistance. Moreover, these findings provide a robust structural and functional foundation, enabling the rational design of targeted inhibitors and restoring colistin activity against serious infections with carbapenem-resistant Enterobacterales (CRE).

Keywords: Alanine scanning mutagenesis; Catalytic mechanism; Colistin resistance; MCR-1; Phosphoethanolamine transferase.

MeSH terms

  • Anti-Bacterial Agents* / pharmacology
  • Colistin* / pharmacology
  • Drug Resistance, Bacterial* / genetics
  • Escherichia coli / drug effects
  • Escherichia coli / genetics
  • Escherichia coli Proteins* / chemistry
  • Escherichia coli Proteins* / genetics
  • Escherichia coli Proteins* / metabolism
  • Ethanolaminephosphotransferase / chemistry
  • Ethanolaminephosphotransferase / genetics
  • Ethanolaminephosphotransferase / metabolism
  • Ethanolamines / chemistry
  • Ethanolamines / metabolism
  • Ethanolamines / pharmacology
  • Lipid A / chemistry
  • Lipid A / metabolism
  • Microbial Sensitivity Tests
  • Molecular Docking Simulation*
  • Mutation
  • Phosphatidylethanolamines

Substances

  • Colistin
  • Anti-Bacterial Agents
  • Escherichia coli Proteins
  • MCR-1 protein, E coli
  • phosphorylethanolamine
  • Phosphatidylethanolamines
  • Lipid A
  • Ethanolaminephosphotransferase
  • phosphatidylethanolamine
  • Ethanolamines