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Genomic Signatures of Coevolution between Nonmodel Mammals and Parasitic Roundworms.

ABSTRACT: Antagonistic coevolution between host and parasite drives species evolution. However, most of the studies only focus on parasitism adaptation and do not explore the coevolution mechanisms from the perspective of both host and parasite. Here, through the de novo sequencing and assembly of the genomes of giant panda roundworm, red panda roundworm, and lion roundworm parasitic on tiger, we investigated the genomic mechanisms of coevolution between nonmodel mammals and their parasitic roundworms and those of roundworm parasitism in general. The genome-wide phylogeny revealed that these parasitic roundworms have not phylogenetically coevolved with their hosts. The CTSZ and prolyl 4-hydroxylase subunit beta (P4HB) immunoregulatory proteins played a central role in protein interaction between mammals and parasitic roundworms. The gene tree comparison identified that seven pairs of interactive proteins had consistent phylogenetic topology, suggesting their coevolution during host-parasite interaction. These coevolutionary proteins were particularly relevant to immune response. In addition, we found that the roundworms of both pandas exhibited higher proportions of metallopeptidase genes, and some positively selected genes were highly related to their larvae's fast development. Our findings provide novel insights into the genetic mechanisms of coevolution between nonmodel mammals and parasites and offer the valuable genomic resources for scientific ascariasis prevention in both pandas.

SUBMITTER: Hu Y

PROVIDER: S-EPMC7826172 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Haemonchus contortus and Teladorsagia circumcincta are among the two most pathogenic internal parasitic nematodes infecting small ruminants, such as sheep and goats, and are a global animal health issue. Accurate identification and delineation of Haemonchidae species is essential for development of diagnostic and control strategies with high resolution for Trichostrongyloidea infection in ruminants. Here, we describe in detail and compare the complete mitochondrial (mt) genomes of the New Zealand H. contortus and T. circumcincta field strains to improve our understanding of species- and strain-level evolution in these closely related roundworms. In the present study, we performed extensive comparative bioinformatics analyses on the recently sequenced complete mt genomes of the New Zealand H. contortus NZ_Hco_NP and T. circumcincta NZ_Teci_NP field strains. Amino acid sequences inferred from individual genes of each of the two mt genomes were compared, concatenated and subjected to phylogenetic analysis using Bayesian inference (BI), Maximum Likelihood (ML), and Maximum Parsimony (MP). The AT-rich mt genomes of H. contortus NZ_Hco_NP and T. circumcincta NZ_Teci_NP are 14,001 bp (A+T content of 77.4%) and 14,081 bp (A+T content of 77.3%) in size, respectively. All 36 of the typical nematode mt genes are transcribed in the forward direction in both species and comprise of 12 protein-encoding genes (PCGs), 2 ribosomal RNA (rrn) genes, and 22 transfer RNA (trn) genes. The secondary structures for the 22 trn genes and two rrn genes differ between H. contortus NZ_Hco_NP and T. circumcincta NZ_Teci_NP, however the gene arrangements of both are consistent with other Trichostrongylidea sequenced to date. Comparative analyses of the complete mitochondrial nucleotide sequences, PCGs, A+T rich and non-coding repeat regions of H. contortus NZ_Hco_NP and T. circumcincta NZ_Teci_NP further reinforces the high levels of diversity and gene flow observed among Trichostrongylidea, and supports their potential as ideal markers for strain-level identification from different hosts and geographical regions with high resolution for future studies. The complete mt genomes of H. contortus NZ_Hco_NP and T. circumcincta NZ_Teci_NP presented here provide useful novel markers for further studies of the meta-population connectivity and the genetic mechanisms driving evolution in nematode species.

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Genomic Signatures of Coevolution between Nonmodel Mammals and Parasitic Roundworms.

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