MATE transport of the E. coli-derived genotoxin colibactin

Nat Microbiol. 2016 Jan 11:1:15009. doi: 10.1038/nmicrobiol.2015.9.

Abstract

Various forms of cancer have been linked to the carcinogenic activities of microorganisms(1-3). The virulent gene island polyketide synthase (pks) produces the secondary metabolite colibactin, a genotoxic molecule(s) causing double-stranded DNA breaks(4) and enhanced colorectal cancer development(5,6). Colibactin biosynthesis involves a prodrug resistance strategy where an N-terminal prodrug scaffold (precolibactin) is assembled, transported into the periplasm and cleaved to release the mature product(7-10). Here, we show that ClbM, a multidrug and toxic compound extrusion (MATE) transporter, is a key component involved in colibactin activity and transport. Disruption of clbM attenuated pks+ E. coli-induced DNA damage in vitro and significantly decreased the DNA damage response in gnotobiotic Il10(-/-) mice. Colonization experiments performed in mice or zebrafish animal models indicate that clbM is not implicated in E. coli niche establishment. The X-ray structure of ClbM shows a structural motif common to the recently described MATE family. The 12-transmembrane ClbM is characterized as a cation-coupled antiporter, and residues important to the cation-binding site are identified. Our data identify ClbM as a precolibactin transporter and provide the first structure of a MATE transporter with a defined and specific biological function.

MeSH terms

  • Animals
  • Crystallography, X-Ray
  • DNA Damage / drug effects
  • Disease Models, Animal
  • Escherichia coli / metabolism*
  • Escherichia coli Infections / microbiology
  • Escherichia coli Infections / pathology
  • Escherichia coli Proteins / chemistry
  • Escherichia coli Proteins / metabolism*
  • Ilex
  • Mice
  • Models, Molecular
  • Mutagens / metabolism*
  • Organic Cation Transport Proteins / chemistry
  • Organic Cation Transport Proteins / metabolism*
  • Peptides / metabolism*
  • Polyketides / metabolism*
  • Protein Conformation
  • Protein Transport
  • Zebrafish

Substances

  • ClbM protein, E coli
  • Escherichia coli Proteins
  • Mutagens
  • Organic Cation Transport Proteins
  • Peptides
  • Polyketides
  • colibactin