Characterization of the complete mitochondrial genomes of the zoonotic parasites Bolbosoma nipponicum and Corynosoma villosum (Acanthocephala: Polymorphida) and the molecular phylogeny of the order Polymorphida

Abstract

Acanthocephalans of the order Polymorphida mainly parasitic in birds and mammals, are of veterinary, medical and economic importance. However, the evolutionary relationships of its 3 families (Centrorhynchidae, Polymorphidae and Plagiorhynchidae) remain under debate. Additionally, some species of Polymorphida (i.e. Bolbosoma spp. and Corynosoma spp.) are recognized as zoonotic parasites, associated with human acanthocephaliasis, but the mitochondrial genomes for representatives of Bolbosoma and Corynosoma have not been reported so far. In the present study, the complete mitochondrial genomes B. nipponicum and C. villosum (Acanthocephala: Polymorphidae) are reported for the first time, which are 14 296 and 14 241 bp in length, respectively, and both contain 36 genes [including 12 PCGs, 22 tRNA genes and 2 rRNA genes] and 2 non-coding regions (NCR1 and NCR2). The gene arrangement of some tRNAs in the mitogenomes of B. nipponicum and C. villosum differs from that found in all other acanthocephalans, except Polymorphus minutus. Phylogenetic results based on concatenated amino acid (AA) sequences of the 12 protein-coding genes (PCGs) strongly supported that the family Polymorphidae is a sister to the Centrorhynchidae rather than the Plagiorhynchidae, and also confirmed the sister relationship of the genera Bolbosoma and Corynosoma in the Polymorphidae based on the mitogenomic data for the first time. Our present findings further clarified the phylogenetic relationships of the 3 families Plagiorhynchidae, Centrorhynchidae and Polymorphidae, enriched the mitogenome data of the phylum Acanthocephala (especially the order Polymorphida), and provided the resource of genetic data for diagnosing these 2 pathogenic parasites of human acanthocephaliasis.

Keywords: Acanthocephala; Bolbosoma; Corynosoma; Polymorphidae; mitochondrial genome; molecular phylogeny; zoonotic parasite.

Graphical abstract

Figure 1.

Gene maps of the mitochondrial genomes of Bolbosoma nipponicum and Corynosoma villosum. All genes are transcribed in the clockwise direction on the same strand, and 22 tRNA genes are designated by the 1-letter code with numbers differentiating each of the 2 tRNAs serine and leucine. The outermost circle shows the GC content and the innermost circle shows the GC skew.

Figure 2.

Relative synonymous codon usage (RSCU) of Bolbosoma nipponicum and Corynosoma villosum. Codon families (in alphabetical order) are provided below the horizontal axis. Values on the top of each bar represent amino acid usage in percentage.

Figure 3.

The predicted secondary structures of 22 tRNAs in the mitogenome of Bolbosoma nipponicum (Watson–Crick bonds indicated by lines, GU bonds indicated by dots, red bases representing anticodons). The tRNAs are labelled with the abbreviations of their corresponding amino acids according to the IUPAC-IUB code.

Figure 4.

The predicted secondary structures of 22 tRNAs in the mitogenome of Corynosoma villosum (Watson–Crick bonds indicated by lines, GU bonds indicated by dots, red bases representing anticodons). The tRNAs are labelled with the abbreviations of their corresponding amino acids according to the IUPAC-IUB code.

Figure 5.

Comparison of the linearized mitochondrial genome arrangement for acanthocephalans species. All genes are transcribed in the same direction from left to right. The tRNAs are labelled by single-letter code for the corresponding amino acid. Bolbosoma nipponicum and Corynosoma villosum are indicated using asterisk (*).

Figure 6.

Phylogenetic analyses of Acanthocephala inferred from ML and BI methods based on concatenated amino acid sequences of 12 PCGs of mitochondrial genomes. Rotaria rotatoria and Philodina citrina were chosen as the out-group. Bootstrap values ⩾70 and Bayesian posterior probabilities values ⩾0.70 are shown in the phylogenetic trees. Bolbosoma nipponicum and Corynosoma villosum are indicated using asterisk (*).