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.

The Nematode Antimicrobial Peptidome: a novel opportunity for parasite control?

“…All species from this clade possess genes encoding Nemapores and GRSPs with only Romanomermis culicivorax possessing Defensin-encoding genes (see Figure 2). Clade 2/I nematodes are generally considered to be more basal and have more limited gene complements for other protein families including neuropeptides, antioxidant enzymes, G-protein-coupled receptors (GPCRs) and ATP-binding cassette transporters (ABC transporters) (McCoy et al, 2014; IHGC 2019; Xu et al, 2020; McKay et al, 2021). The reduced AMP arsenal observed in Clade 2/I may indicate that elevated AMP diversity in the Crown Clades (Clade 8-12) originated as a result of gene duplications and/or selective pressures that are not observed in the basal clades.…”

Genus-level evolutionary relationships of FAR proteins reflect the diversity of lifestyles of free-living and parasitic nematodes

“…Our previous study showed that the proportion of the duplicated BUSCOs (13.1–36.7%) in four mitotic parthenogenetic species was higher than in three meiotic parthenogenetic species (0.4–3.0%). The ratio of these BUSCOs number in root-knot nematodes to M. hapla with 2:1 or 3:1 reached to 26–42% in four mitotic parthenogenetic species, particularly in M. arenaria , while was less than 5% in two meiotic parthenogenetic species [ 34 ] . Thus, the multi-copy nature of far gene in mitotic parthenogenetic species was likely due to their genomic characteristics.…”

“…Genome assemblies of 58 nematodes were retrieved from Wormbase WBPS10 [ 64 ]. We filtered fragmental genome according to assembly metrics and kept one high-quality assembly for multi-assembly species as described [ 34 ]. We employed the same pipeline to identify FAR proteins in nematode genomes [ 34 ].…”

“…We filtered fragmental genome according to assembly metrics and kept one high-quality assembly for multi-assembly species as described [ 34 ]. We employed the same pipeline to identify FAR proteins in nematode genomes [ 34 ]. We downloaded Gp-FAR-1 sequence from the Swissprot database as query in a homology search of the nematode genomes using HMMSEARCH with parameters 1e-3.…”

A Complex Proteomic Response of the Parasitic Nematode Anisakis simplex s.s. to Escherichia coli Lipopolysaccharide

“…Xu et al. ( 87 ) reported a higher expression of prdx-2 than prdx-3 in developmental stages of C. elegans . It has been also reported that prdx-2 from C. elegans is more important for protecting against H 2 O 2 than prdx-3 ( 88 ), what is consistent with our results ( Fig.…”