A gene horizontally transferred from bacteria protects arthropods from host plant cyanide poisoning.
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.
Laboratory of Agrozoology, Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium.
Nicky
N
Wybouw
Laboratory of Agrozoology, Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium.
Wannes
W
Dermauw
Laboratory of Agrozoology, Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium.
Luc
L
Tirry
SynBioC Research Group, Department of Sustainable Organic Chemistry and Technology, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium.
Christian
C
Stevens
Department of Biology, University of Western Ontario, London, Canada Instituto de Ciencias de la Vid y el Vino, Logroño, Spain.
Miodrag
M
Grbić
Institut National de la Recherche Agronomique, Centre National de la Recherche Scientifique and Université de Nice Sophia Antipolis, Nice, France.
René
R
Feyereisen
Laboratory of Agrozoology, Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, Netherlands thomas.vanleeuwen@ugent.be.
Thomas
T
Van Leeuwen
D000409:Alanine / Q000031:analogs & derivatives / Q000378:metabolism; D000818:Animals; D030801:Animals, Genetically Modified; D001419:Bacteria / Q000235:genetics*; D003547:Cysteine Synthase / Q000235:genetics / Q000378:metabolism; D020869:Gene Expression Profiling; D022761:Gene Transfer, Horizontal; D006027:Glycosides / Q000378:metabolism*; D006856:Hydrogen Cyanide / Q000633:toxicity; D008190:Lyases / Q000235:genetics / Q000378:metabolism; D010802:Phylogeny; D040102:Tetranychidae / Q000235:genetics*; D014158:Transcription, Genetic
D006027:Glycosides; D006856:Hydrogen Cyanide; C004631:3-cyanoalanine; D003547:Cysteine Synthase; D008190:Lyases; C019955:beta-cyanoalanine synthase; D000409:Alanine
Tetranychus urticae; cyanogenesis; lateral gene transfer; phytophagy