A large transposable element mediates metal resistance in the fungus Paecilomyces variotii

The horizontal transfer of large gene clusters by mobile elements is a key driver of prokaryotic adaptation in response to environmental stresses. Eukaryotic microbes face similar stresses; however, a parallel role for mobile elements has not been established. A stress faced by many microorganisms is toxic metal ions in their environment. In fungi, identified mechanisms for protection against metals generally rely on genes that are dispersed within an organism’s genome. Here, we discover a large (∼85 kb) region that confers tolerance to five metal/metalloid ions (arsenate, cadmium, copper, lead, and zinc) in the genomes of some, but not all, strains of a fungus, Paecilomyces variotii. We name this region HEPHAESTUS (Hφ) and present evidence that it is mobile within the P. variotii genome with features characteristic of a transposable element. HEPHAESTUS contains the greatest complement of host-beneficial genes carried by a transposable element in eukaryotes, suggesting that eukaryotic transposable elements might play a role analogous to bacteria in the horizontal transfer of large regions of host-beneficial DNA. Genes within HEPHAESTUS responsible for individual metal tolerances include those encoding a P-type ATPase transporter—PcaA—required for cadmium and lead tolerance, a transporter—ZrcA—providing tolerance to zinc, and a multicopper oxidase—McoA—conferring tolerance to copper. In addition, a subregion of Hφ confers tolerance to arsenate. The genome sequences of other fungi in the Eurotiales contain further examples of HEPHAESTUS, suggesting that it is responsible for independently assembling tolerance to a diverse array of ions, including chromium, mercury, and sodium. •A gene cluster in the fungus Paecilomyces variotii confers metal resistance•The gene cluster displays hallmarks of coordinated movement as a mobile element•The cluster is variably located in different genomic locations in different strains•HEPHAESTUS is an example of transposons carrying beneficial traits in eukaryotes Urquhart et al. report a new genetic element in the fungus Paecilomyces variotii and show that it includes many genes conferring protection from toxic levels of metal ions. The element, termed HEPHAESTUS, has all the hallmarks of being a large eukaryotic transposon, and other examples are found in the genomes of other fungi.