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

Published online by Cambridge University Press:  10 October 2018

D. S. Zarlenga Open the ORCID record for D. S. Zarlenga [Opens in a new window] ,
M. Mitreva ,
P. Thompson ,
R. Tyagi ,
W. Tuo Open the ORCID record for W. Tuo [Opens in a new window]  and
E. P. Hoberg
D. S. Zarlenga*
Affiliation:
USDA, Agricultural Research Service, Animal Parasitic Diseases Lab, Beltsville, MD 20705USA
M. Mitreva
Affiliation:
The Genome Institute, Washington University School of Medicine, St. Louis, MO 63108, USA
P. Thompson
Affiliation:
USDA, Agricultural Research Service, Animal Parasitic Diseases Lab, Beltsville, MD 20705USA
R. Tyagi
Affiliation:
The Genome Institute, Washington University School of Medicine, St. Louis, MO 63108, USA
W. Tuo
Affiliation:
USDA, Agricultural Research Service, Animal Parasitic Diseases Lab, Beltsville, MD 20705USA
E. P. Hoberg
Affiliation:
USDA, Agricultural Research Service, Animal Parasitic Diseases Lab, Beltsville, MD 20705USA
*
Author for correspondence: D. S. Zarlenga, E-mail: [email protected]
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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, is present in more than 35 members of the Phylum Nematoda, but absent from free-living and clade V organisms. Phylogenetic analyses showed that the cyanases of clade I organisms Trichinella spp., Trichuris spp. and Soboliphyme baturini (Subclass: Dorylaimia) represent a well-supported monophyletic clade with plant cyanases. In contrast, all cyanases found within the Subclass Chromadoria which encompasses filarioids, ascaridoids and strongyloids are homologous to those of bacteria. Western blots exhibited typical multimeric forms of the native molecule in protein extracts of Trichinella spiralis muscle larvae, where immunohistochemical staining localized the protein to the worm hypodermis and underlying muscle. Recombinant Trichinella cyanase was bioactive where gene transcription profiles support functional activity in vivo. Results suggest that: (1) independent HGT in parasitic nematodes originated from different Kingdoms; (2) cyanase acquired an active role in the biology of extant Trichinella; (3) acquisition occurred more than 400 million years ago (MYA), 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.

Keywords

Cyanaseevolutionhorizontal gene transfernematodeparasitismTrichinella
Type
Research Article
Information
Parasitology , Volume 146 , Issue 4 , April 2019 , pp. 445 - 452
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Copyright
Copyright © Cambridge University Press 2018 

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