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

PLoS Negl Trop Dis. 2019 Nov 21;13(11):e0007846. doi: 10.1371/journal.pntd.0007846. eCollection 2019 Nov.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Biological*
  • Angiostrongylus cantonensis / classification*
  • Angiostrongylus cantonensis / genetics*
  • Angiostrongylus cantonensis / isolation & purification
  • Animals
  • China
  • Computational Biology
  • Evolution, Molecular*
  • Gene Expression Profiling
  • Genome, Helminth*
  • High-Throughput Nucleotide Sequencing
  • Humans
  • Rodentia
  • Strongylida Infections / parasitology*
  • Strongylida Infections / veterinary*
  • Trematoda

Grants and funding

ZD-W received grants from National Research and Development Plan of China (2016YFC1200500), the Major Basic Research of Ministry of Science and Technology of China (973 Project) (No.2010CB530000), National Natural Science Foundation of China (No.81261160324, No.81271855, and No.81371836), Science and Technology Planning Project of Guangdong Province (No.2016A050502008), Natural Science Foundation of Guangdong Province, China (No. 2015A030310058) and the 111 Project (Grant No. B12003). ZY-L received a grant from National Natural Science Foundation of China (No. 81572023) and Science and Technology Planning Project of Guangdong Province (2019B030316025). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.