A tale of three kingdoms: members of the Phylum Nematoda independently acquired the detoxifying enzyme cyanase through horizontal gene transfer from plants and bacteria

Authors: Zarlenga, Dante; MITREVA, MAKEDONKA - Washington University School Of Medicine; THOMPSON, PETER - Non ARS Employee; TYAGI, R - Washington University School Of Medicine; Tuo, Wenbin; Hoberg, Eric

Submitted to: Parasitology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/13/2018
Publication Date: 1/1/2018
Citation: Zarlenga, D.S., Mitreva, M., Thompson, P., Tyagi, R., Tuo, W., Hoberg, E.P. 2018. A tale of three kingdoms: members of the Phylum Nematoda independently acquired the detoxifying enzyme cyanase through horizontal gene transfer from plants and bacteria. Parasitology. 146(4):445-452. https://doi.org/10.1017/S0031182018001701.
DOI: https://doi.org/10.1017/S0031182018001701

Interpretive Summary: Parasitism among nematodes occurred undependably at least 13 times over evolution. Understanding the evolutionary history of nematodes will help to identify and characterize commonalities in how they became parasites. One key mechanism and driving force for host adaptation is the acquisition of genes present in lower level organisms by more advanced organisms that have a commensal or mutual association with the lower organism; this is referred to as Horizontal Gene Transfer (HGT). Initially by database analysis and subsequently by biochemical experimentation, the gene cyanase, typically found only in plants, bacteria, and fungi, was identified in a very small subclass of parasitic nematodes. Cyanase is an enzyme that catalyzes the breakdown of cyanate to ammonia and carbon dioxide and likely played a role during primordial evolution. The unique finding was that the gene acquired by the oldest of nematode groups i.e., Trichinella, Trichuris, Soboliphyme, was acquired from plants whereas the cyanase gene from more recently evolved nematodes was acquired from bacteria. Second, the results suggest that the last common ancestor of these animal parasites had an association with plants and this association likely occurred 450 million years ago when terrestrial plants first made their way onto land. Finally, these data may provide a link between this gene, host adaptation and the acquisition of parasitism in these organisms. This information is important to scientists trying to better understand the evolution of parasitism among nematodes.

Technical Abstract: Horizontal gene transfer (HGT) has played an important role in the evolution of nematodes. Among candidate genes, cyanase, which is typically found only in plants, bacteria and fungi, was present in more than 35 members of the Phylum Nematoda, but absent from free-living worms and organisms of the crown clades. Phylogenetic analyses showed that the cyanase among clade I organisms Trichinella spp., Trichuris spp., and Soboliphyme baturini, (Subclass: Dorylaimia) formed a well-supported monophyletic clade with plant cyanases. In contrast, all cyanases found within the Subclass Chromadoria were homologous with those of bacteria. Western blots exhibited typical multimeric forms of the native protein in protein extracts of T. spiralis muscle larvae where immunohistochemical staining localized the protein to the worm hypodermis and underlying muscle. A recombinant Trichinella cyanase generated a bioactive protein where gene transcription profiles support functional activity in vivo. Results suggest that: 1) independent HGT occurred in parasitic nematodes with origins from different Kingdoms; 2) cyanase acquired an active role in the biology of extant Trichinella; 3) acquisition occurred over 400 million years ago prior to the divergence of the Trichinellida and Dioctophymatida, and 4) early, free-living ancestors of the genus Trichinella had an association with terrestrial plants.