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

• Published in: eLife Vol. 3; p. e02365
• Main Authors: Wybouw, Nicky, Dermauw, Wannes, Tirry, Luc, Stevens, Christian, Grbić, Miodrag, Feyereisen, René, Van Leeuwen, Thomas
• Format: Journal Article
• Language: English
• Published: England eLife Sciences Publications Ltd 24.04.2014; eLife Sciences Publication; eLife Sciences Publications, Ltd
• Subjects: Alanine - analogs & derivatives; Alanine - metabolism; Amino acids; Animals; Animals, Genetically Modified; Arthropoda; Arthropods; Bacteria; Bacteria - genetics; Biosynthesis; cyanogenesis; Cysteine synthase; Cysteine Synthase - genetics; Cysteine Synthase - metabolism; Detoxification; Environmental Sciences; Enzymes; Flowers & plants; Gene expression; Gene Expression Profiling; Gene Transfer, Horizontal; Genomics and Evolutionary Biology; Glucosides; Glycosides - metabolism; Herbivores; Horizontal transfer; Host plants; Hydrogen cyanide; Hydrogen Cyanide - toxicity; L-3-Cyanoalanine synthase; lateral gene transfer; Life Sciences; Lyases - genetics; Lyases - metabolism; Phylogeny; phytophagy; Plant protection; Sulfur; Tetranychidae - genetics; Tetranychus urticae; Transcription, Genetic; Tetranychus urticae; phytophagy; cyanogenesis; lateral gene transfer
• DOI: 10.7554/eLife.02365
• ISSN: 2050-084X

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. Hydrogen cyanide is a poison that is deadly for most forms of life. Also known as prussic acid, it has killed countless humans throughout history in accidents and during the Holocaust. Hydrogen cyanide is also used by plants to defend themselves against insects and other herbivorous animals. Many plants produce chemicals called cyanogenic glycosides that can be converted into hydrogen cyanide when the plant is eaten. This is an ancient and efficient defense against all sorts of herbivores, including humans. For instance, cassava is a key source of food in sub-Saharan Africa and South America, but it contains cyanogenic glucosides and is highly toxic if eaten in unprocessed form. However, some insects and mites can thrive on cyanogenic plants, often to the extent of becoming pests on these plants. Certain moths, such as burnet moths, have gone further and now depend on cyanogenic glucosides for their own defenses against predators such as birds. How these mites and insects are capable of fending off cyanide toxicity has long remained a mystery. Now Wybouw et al. have identified a mite enzyme that detoxifies hydrogen cyanide to produce a compound called beta-cyanoalanine. Remarkably, the DNA that encodes this enzyme did not evolve in animals but originally belonged to a bacterium. Wybouw et al. show that the gene was transferred to the genome of the spider mite Tetranychus urticae perhaps a few hundred million years ago. An equivalent gene was also found in moths and butterflies, which explains why these insects can thrive on plants that produce hydrogen cyanide. This lateral gene transfer from bacteria to animals is a remarkable coalition of two kingdoms against another, and illustrates a new aspect of the chemical warfare between plants and animals. This study also increases our awareness of the importance of laterally transferred genes in the genomes of higher organisms.