Characterization of the complete mitogenome of Centrorhynchus clitorideus (Meyer, 1931) (Palaeacanthocephala: Centrorhynchidae), the largest mitochondrial genome in Acanthocephala, and its phylogenetic implications

https://doi.org/10.1016/j.molbiopara.2020.111274Get rights and content

Highlights

  • The complete mt genome of Centrorhynchus clitorideus was sequenced for the first time.

  • The mt genome of C. clitorideus encodes the 36 putative genes typically found in acanthocephalans.

  • With 15,884 bp in length, the mt genome of C. clitorideus is the largest of any acanthocephalan reported to date.

  • Phylogenetic analysis supports monophyly of Palaeacanthocephala, but rejects monophyly of Echinorhynchida.

  • The phylogeny indicates that Sphaerirostris should be relegated to a junior synonym of Centrorhynchus.

Abstract

Species of Centrorhynchus (Polymorphida: Centrorhynchidae) commonly parasitize various falconiform and strigiform birds worldwide. In the present study, the complete mitochondrial (mt) genome sequences of Centrorhynchus clitorideus was sequenced and annotated for the first time based on specimens collected from the little owl Athene noctua (Scopoli) (Strigiformes: Strigidae) in Pakistan. The complete mt genome sequences of C. clitorideus is 15,884 bp in length, and contained 36 genes [two rRNA genes (rrnL and rrnS), 22 tRNA genes and 12 protein-coding genes (PCGs) (lacking atp8)] and two non-coding regions (NCR1 and NCR2), which represents the largest mt genome of acanthocephalan reported so far. In order to assess the systematic position of C. clitorideus and the interrelationship of the family Centrorhynchidae and the other families in order Polymorphida, the phylogenetic tree was constructed using Bayesian inference (BI) based on amino acid sequences of 12 PCGs. Phylogenetic results supported C. clitorideus formed a sister relationship to C. milvus in Centrorhynchidae, which has a sister relationship to the representatives of Polymorphidae + Plagiorhynchidae. Our results revealed the monophyly of Polymorphida and paraphyly of Echinorhynchida in the class Palaeacanthocephala. The validity of the genus Sphaerirostris (Polymorphida: Centrorhynchidae) was also challenged by our phylogenetic results, which seems to be a synonym of Centrorhynchus. Moreover, the present phylogenetic analysis indicated that the family Quadrigyridae and subfamily Pallisentinae (A. cheni and P. celatus) are polyphyletic.

Introduction

The phylum Acanthocephala is currently divided into four classes, including Archiacanthocephala, Eoacanthocephala, Palaeacanthocephala and Polyacanthocephala, with about 1300 nominal species reported worldwide [1,2]. Among them, Palaeacanthocephala includes three orders, namely Echinorhynchida, Polymorphida and Heteramorphida, with more than 840 species mainly parasitic in the intestine of birds and fishes, commonly using arthropod (i.e. insects, amphipods, isopods, copepods or ostracods) as intermediate hosts [[2], [3], [4], [5], [6], [7], [8]].

Recently, some authors have made efforts to establish the phylogenetic relationships of the four classes in Acanthocephala, and also to solve particular systematic problems of high taxa level in Palaeacanthocephala using the mitochondrial (mt) genome sequence data [[9], [10], [11], [12], [13], [14], [15]]. However, due to the paucity of mt genome sequences for most of family-level taxa in Palaeacanthocephala, these mitogenomic phylogenetic studies have included only a very small representatives of the diversity of Palaeacanthocephala. The phylogenetic relationships of the three orders Echinorhynchida, Polymorphida and Heteramorphida and the systematic status of some families in Palaeacanthocephala remains unsolved. Our knowledge of the phylogeny of Acanthocephala, especially the Palaeacanthocephala, is still far from comprehensive.

In the present study, the complete mt genome sequences of Centrorhynchus clitorideus (Palaeacanthocephala: Centrorhynchidae) was sequenced and annotated for the first time based on specimens collected from the little owl Athene noctua (Scopoli) (Strigiformes: Strigidae) in Pakistan. In order to assess the systematic position of C. clitorideus and the phylogenetic relationship of the family Centrorhynchidae and the other families in the order Polymorphida, the phylogenetic tree was constructed using Bayesian inference (BI) based on amino acid sequences of 12 protein-coding regions (PCGs).

Section snippets

Parasite collection

A total of 12 adult specimens of C. clitorideus were isolated from the intestine of the little owl (Athene noctua) in the district Swabi (34°07′07.23" N, 72°36'32.38" E), in Pakistan. Specimens were washed carefully in saline water and then kept in water for whole night until the proboscis everted, and then stored in 70 % ethanol at −20 °C for further use. Specimens were identified to species level based on morphological characters such as, the size and morphology of trunk, proboscis, proboscis

Genome organization and base composition

The complete mt genome of C. clitorideus is 15,884 bp in size (GenBank accession no. MT113355), which is the largest mt genome compared to the other acanthocephalan species reported so far, and contains all 36 genes: 2 rRNA genes (rrnL and rrnS), 22 tRNA genes and 12 PCGs (lacking atp8) with two non-coding region (Fig. 1). In Acanthocephala, the lack of atp8 gene is common [11,14], but Leptorhynchoides thecatus (Rhadinorhynchidae) has two putative atp8 genes [31]. Genes are either separated by

Phylogeny

The representatives of Acanthocephala were divided into three major clades, which represent the classes Archiacanthocephala, Palaeacanthocephala and Eoacanthocephala + Polyacanthocephala, with a high nodal support (BPP = 1) (Fig. 3). The class Archiacanthocephala, including O. luehei and M. hirudinaceus, is at the most basal position of the phylogenetic analysis, which shows a sister relationship to Palaeacanthocephala + Eoacanthocephala + Polyacanthocephala. This result agreed well with the

Conclusions

In this study, we characterized the complete mt genome sequences of Centrorhynchus clitorideus for the first time based on specimens collected from the little owl Athene noctua (Scopoli) (Strigiformes: Strigidae) in Pakistan. The complete mt genome sequences of C. clitorideus is 15,884 bp in length and represents the largest mt genome of acanthocephalan reported so far. Phylogenetic analysis based on concatenated inferred amino acid sequences strongly supported C. clitorideus formed a sister

Author contribution

JM, XQZ and LL conceived and designed the study, and critically revised the manuscript. NM performed the experiment, analyzed the data and drafted the manuscript. MSK participated in specimen collections. Suleman, QZ and HU contributed to data analysis and preparation of figures. All authors read and approved the final manuscript.

Declaration of Competing Interest

The authors declare that they have no conflicts of interest with the contents of this article.

Acknowledgments

This study was supported by the National Natural Science Foundation of China (Grant nos. 31872197 and 31702225), the International Science and Technology Cooperation Project of Gansu Provincial Key Research and Development Program (Grant No. 17JR7WA031), the Elite Program of Chinese Academy of Agricultural Sciences, the Agricultural Science and Technology Innovation Program (ASTIP) (Grant No. CAAS-ASTIP-2016-LVRI-03), the Strategic Priority Research Program of the Chinese Academy of Sciences (

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