Speciation and adaptive evolution reshape antioxidant enzymatic system diversity across the phylum Nematoda

Abstract

Background: Nematodes have evolved to survive in diverse ecological niches and can be a serious burden on agricultural economy, veterinary medicine, and public health. Antioxidant enzymes in parasitic nematodes play a critical role in defending against host oxidative stress. However, the features of the evolution of antioxidant enzymes in the phylum Nematoda remain elusive. Results: Here, we systematically investigated the evolution and gene expression of antioxidant enzymes in the genomes of 59 nematodes and transcriptomes of 20 nematodes. Catalase has been independently lost in several orders, suggesting that it is unnecessary for some nematodes. Unlike in mammals, phospholipid hydroperoxide glutathione peroxidase is widely distributed in nematodes, among which it has evolved independently. We found that superoxide dismutase (SOD) has been present throughout nematode evolutionary process, and the extracellular isoform (SOD3) is diverged from the corresponding enzyme in mammals and has undergone duplication and differentiation in several nematodes. Moreover, the evolution of intracellular and extracellular SOD isoforms in filaria strongly indicates that extracellular SOD3 originated from intracellular SOD1 and underwent rapid evolution to form the diversity of extracellular SOD3. We identify a novel putative metal-independent extracellular SOD presenting independently in Steinernema and Strongyloididae lineage that featured a high expression level in Strongyloides larvae. Sequence divergence of SOD3 between parasitic nematodes and their closest free-living nematode, the specifically high expression in the parasitic female stage, and presence in excretory-secretory proteome of Strongyloides suggest that SOD3 may be related with parasitism. Conclusions: This study advances our understanding of the complex evolution of antioxidant enzymes across Nematoda and provides targets for controlling parasitic nematode diseases.