Speciation and adaptive evolution reshape antioxidant enzymatic system diversity across the phylum Nematoda
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RESEARCH ARTICLE
Open Access
Speciation and adaptive evolution reshape antioxidant enzymatic system diversity across the phylum Nematoda Lian Xu1,2†, Jian Yang1†, Meng Xu3†, Dai Shan4, Zhongdao Wu2* and Dongjuan Yuan5*
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. Keywords: Antioxidant enzyme, Extracellular superoxide dismutase, Gene family evolution, Nematoda, Transcriptome
* Correspondence: [email protected]; [email protected] † Lian Xu, Jian Yang and Meng Xu contributed equally to this work. 2 Department of Parasitology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510080, China 5 College of Veterinary Medicine, South China Agricultural University, Guangzhou 510642, China Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes w
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