The genetic basis of adaptive evolution in parasitic environment from the Angiostrongylus cantonensis genome

Abstract

Angiostrongylus cantonensis (rat lungworm) is the etiological agent of angiostrongyliasis, mainly causing eosinophilic meningitis or meningoencephalitis in human. Although the biology of A. cantonensis is relatively well known, little is understood about the mechanisms of the parasite’s development and survival in definitive hosts, or its adaptation to a broad range of snail intermediate hosts. Here, we generate a high-quality assembly of a well-defined laboratory strain of A. cantonensis from Guangzhou, China, by using Illumina and PacBio sequencing technologies. We undertake comparative analyses with representative helminth genomes and explore transcriptomic data throughout key developmental life-cycles of the parasite. We find that part of retrotransposons and gene families undergo multiple waves of expansions. These include extracellular superoxide dismutase (EC-SOD) and astacin-like proteases which are considered to be associated with invasion and survival of the parasite. Furthermore, these paralogs from different sub-clades based on phylogeny, have different expression patterns in the molluscan and rodent stages, suggesting divergent functions under the different parasitic environment. We also find five candidate convergent signatures in the EC-SOD proteins from flukes and one sub-clade of A. cantonensis. Additionally, genes encoding proteolytic enzymes, involved in host hemoglobin digestion, exhibit expansion in A. cantonensis as well as two other blood-feeding nematodes. Overall, we find several potential adaptive evolutionary signatures in A. cantonensis, and also in some other helminths with similar traits. The genome and transcriptomes provide a useful resource for detailed studies of A. cantonensis-host adaptation and an in-depth understanding of the global-spread of angiostrongyliasis.

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

“…It can infer that extracellular Cu/Zn SOD might be easily secreted into the extracellular matrix or ES for defense against host ROS. Lineage-specific expansion was found in Angiostrongylus and was absent in its close taxa, and relatively high expression was found in the snail-borne stage, all of which support our previous hypothesis that lineage-specific expansion of SOD3 may promote its survival in its snail host [22].…”

“…4 a). Available public RNA-seq datasets [ 13 , 22 ] showed expression specificity (tissue specificity index τ ≥ 0.8) at a certain stage of most lineage-expansion of SOD3 isoforms in T. canis (seven out of seven) and A. cantonensis (five out of eight) (Fig. 4 a, Additional file 6 : Table S6).…”

“…The number of antioxidant enzyme in nematodes, unlike the number in mammals, varies in different clades, specifically in Clades III, IV, and V. It has been estimated that the split between Clade III, and Clades IV and V was about 280 mya [ 22 ], when oxygen levels increased (oxygen data were retrieved from the TimeTree database [ 56 ], Fig. 7 ).…”

“…In all, 103 nematode assemblies (86 species), not including A. cantonensis [ 22 ] and N. brasiliensis [ 34 ], were retrieved from Wormbase WBPS10 [ 68 ]. We filtered parasitic species with low assembly metrics (Scaffold N50 and Contig N50 < 1 kb), and we retained one high-quality assembly for species with multi-assemblies.…”

“…An increasing number of genomes of free-living and parasitic nematodes are being sequenced [10], particularly those of three major soil-transmitted nematodes, ascaris [10][11][12][13], hookworms [10,14,15], and whipworms [16,17]; the vector-borne nematodes Anisakis simplex [10] (herring worm), filarial worms [10,[18][19][20][21], Angiostrongylus [10,22], and Dracunculus medinensis [10] (guinea worm); and the parthenogenetic parasite Strongyloides [23]. Extensive genomic and transcriptomic data have allowed us to explore the growth, reproduction, metabolism, and parasitism of parasites, but this has had far-reaching guiding significance for the prevention and control of parasitic diseases that can seriously harm human and animal health and economic crop growth.…”