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. 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. This study advances our understanding of the complex evolution of antioxidant enzymes across Nematoda and provides targets for controlling parasitic nematode diseases.

中文翻译：

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形态和适应性进化重塑线虫门上的抗氧化剂酶系统多样性

线虫已经进化为能够在各种生态位中生存，并且可能成为农业经济，兽医和公共卫生的沉重负担。寄生线虫中的抗氧化酶在防御宿主氧化应激中起关键作用。但是，线虫门中抗氧化酶的进化特征仍然难以捉摸。在这里，我们系统地研究了59个线虫基因组和20个线虫转录组中抗氧化酶的进化和基因表达。过氧化氢酶已经以几个顺序独立丢失，表明某些线虫没有必要。与哺乳动物不同，磷脂氢过氧化物谷胱甘肽过氧化物酶广泛分布于线虫中，其中已独立进化。我们发现超氧化物歧化酶（SOD）已经存在于整个线虫的进化过程中，并且胞外亚型（SOD3）与哺乳动物中的相应酶分叉，并且已经在多个线虫中进行了复制和分化。此外，丝虫中细胞内和细胞外SOD同工型的进化强烈表明，细胞外SOD3起源于细胞内SOD1并经历了快速进化以形成细胞外SOD3的多样性。我们确定了一种新型推定的金属独立的细胞外SOD，在Steinernema和Strongyloididae谱系中独立存在，其在Strongyloides幼虫中具有高表达水平。寄生线虫与其最接近的自由生活线虫之间的SOD3序列差异，在寄生雌虫阶段特别高的表达，并且存在强链霉菌的分泌-分泌蛋白质组表明，SOD3可能与寄生虫有关。这项研究提高了我们对整个线虫中抗氧化酶的复杂进化的理解，并为控制寄生线虫疾病提供了目标。