A gene horizontally transferred from bacteria protects arthropods from host plant cyanide poisoning

Elife. 2014 Apr 24:3:e02365. doi: 10.7554/eLife.02365.

Abstract

Cyanogenic glucosides are among the most widespread defense chemicals of plants. Upon plant tissue disruption, these glucosides are hydrolyzed to a reactive hydroxynitrile that releases toxic hydrogen cyanide (HCN). Yet many mite and lepidopteran species can thrive on plants defended by cyanogenic glucosides. The nature of the enzyme known to detoxify HCN to β-cyanoalanine in arthropods has remained enigmatic. Here we identify this enzyme by transcriptome analysis and functional expression. Phylogenetic analysis showed that the gene is a member of the cysteine synthase family horizontally transferred from bacteria to phytophagous mites and Lepidoptera. The recombinant mite enzyme had both β-cyanoalanine synthase and cysteine synthase activity but enzyme kinetics showed that cyanide detoxification activity was strongly favored. Our results therefore suggest that an ancient horizontal transfer of a gene originally involved in sulfur amino acid biosynthesis in bacteria was co-opted by herbivorous arthropods to detoxify plant produced cyanide.DOI: http://dx.doi.org/10.7554/eLife.02365.001.

Keywords: Tetranychus urticae; cyanogenesis; lateral gene transfer; phytophagy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alanine / analogs & derivatives
  • Alanine / metabolism
  • Animals
  • Animals, Genetically Modified*
  • Bacteria / genetics*
  • Cysteine Synthase / genetics
  • Cysteine Synthase / metabolism
  • Gene Expression Profiling
  • Gene Transfer, Horizontal*
  • Glycosides / metabolism*
  • Hydrogen Cyanide / toxicity
  • Lyases / genetics
  • Lyases / metabolism
  • Phylogeny
  • Tetranychidae / genetics*
  • Transcription, Genetic

Substances

  • Glycosides
  • Hydrogen Cyanide
  • 3-cyanoalanine
  • Cysteine Synthase
  • Lyases
  • beta-cyanoalanine synthase
  • Alanine

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.