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. 2026 Mar 10;125(1):38. doi: 10.1007/s00436-026-08633-1

The mitochondrial genome characteristics of Coronocyclus coronatus (Looss, 1900) and comparative analysis with other strongylid nematodes

Yan Hao 1, Yinghao Xia 1, Liqun Ma 2, Zhe Hao 3, Bing Li 1, Yanzhen Bu 2,✉
PMCID: PMC12975830  PMID: 41803334

Abstract

As important equine parasites, strongylid nematodes can cause severe health impairments and economic losses in the livestock industry. Current control strategies primarily rely on anthelmintic drugs. Therefore, elucidating the characteristics of its mitochondrial genomes not only clarifies the evolutionary mechanisms of strongylid nematodes but also provides a molecular-level theoretical basis for developing environmentally adaptive control strategies. In this study, the complete mitochondrial genome of Coronocyclus coronatus was sequenced and analyzed using next-generation sequencing technology. Results revealed a 13,870 bp circular double-stranded molecule containing 12 protein-coding genes, 22 tRNA genes, 2 rRNA genes, and 2 non-coding regions, with a high AT content (74.75%) indicating significant AT bias. Among the 12 protein-coding genes, ATT, TTG, and ATA served as start codons. All genes terminated with complete TAA or TAG stop codons, except for COX3 which used an incomplete T stop codon. Phylogenetic analysis revealed closer affinity of C. coronatus with Cylicocyclus than with other Coronocyclus species. This study enriches mitochondrial genome data for strongylid nematodes, providing a foundation for resolving the taxonomic status and molecular evolution of Strongylidae.

Supplementary Information

The online version contains supplementary material available at 10.1007/s00436-026-08633-1.

Keywords: Coronocyclus coronatus, Strongylid nematodes, Mitochondrial genome, Phylogenetic analysis

Introduction

Strongylid nematodes are an important threat to the health of equidae animals. Studies indicate widespread prevalence of strongyle infections across multiple countries and regions, including China, Australia, Poland, Thailand, Brazil, and South Africa(Gao et al. 2021; Abbas et al. 2023; Boisseau et al. 2023; Hamad et al. 2024; Soutello et al. 2025). These infections substantially compromise equine health and productivity, with infected hosts exhibiting clinical signs such as colic, anorexia, dyspepsia, weight loss, and severe anemia. In extreme cases, mortality may occur, resulting in considerable economic losses to the livestock industry (Love et al. 1999; Kay et al. 2019; Jota Baptista et al. 2021).

Coronocyclus coronatus belongs to the genus Coronocyclus within the subfamily Cyathostominae of the family Strongylidae. As a significant pathogen causing strongylosis, it often co-occurs with other species of strongylid nematodes in the intestinal tract of equidae animals (Lichtenfels et al. 2008; Clark et al. 2018). It exhibits a prominent buccal collar, with an external leaf-crown composed of 22 leaf-like elements, while the internal leaf-crown contains approximately two to three times as many elements as the external one. Males have a well-developed copulatory bursa and a short genital cone. Females have a vulva anterior to the anus, a straight tail, and a digitiform tip.

Currently, research on C. coronatus by scholars worldwide has mainly focused on morphological characteristics, life history, epidemiology, disease prevention and control, and molecular identification (Morariu et al. 2016; Bredtmann et al. 2019; Abbas et al. 2023). With the advancement of molecular biology, there have been increasing reports on evolution and phylogeny using single genes such as ribosomal ITS sequences, mitochondrial COI, and ND1 to explore species evolution and genetic relationships. Bu et al. (2012) amplified, sequenced and analyzed the ITS regions of three nematode species including C. coronatus via PCR, demonstrating that ITS sequences could serve as reliable molecular markers for the identification of Coronocyclus. Using both ITS-2 and COI molecular markers, Bredtmann et al. (2019) further revealed a close phylogenetic relationship between C. coronatus and Cylicostephanus calicatus. However, the complete mitochondrial genome (mt genome) of C. coronatus has not been reported. Compared to single genes, the mt genome exhibits characteristics such as a simple structure, small size, rapid evolutionary rate, low recombination rate, high copy number, and maternal inheritance (Hu and Gasser 2006). These characteristics make it a valuable molecular marker widely used in research areas including species classification, population structure, genetic variation, and phylogenetics (Gao et al. 2022; Song et al. 2022; Yang and Duan 2024).

Despite these efforts, knowledge regarding the mt genome of C. coronatus remains limited, and its evolutionary relationship with other strongylid nematodes is still unclear. This study used next-generation sequencing technology to sequence the mt genome of C. coronatus and conducted comparative analyses with other published strongylid mt genomes to investigate its structural features, codon usage bias, and phylogenetic relationships. The results will fill this knowledge gap in mt genome data on C. coronatus and provide a crucial theoretical basis for strongylid taxonomy, species evolution mechanisms, mitochondrial genomic characteristics, and phylogenetic relationships among other strongylid nematodes. Additionally, this study lays the groundwork for developing new molecular diagnostic methods and control strategies.

Materials and methods

Sample collection and DNA extraction

Adult Coronocyclus coronatus were collected from the intestinal contents of donkeys at a slaughterhouse in Xinxiang City, Henan Province. The collected nematodes were repeatedly rinsed with physiological saline to remove impurities. Preliminary species identification was performed based on morphological characteristics (Lichtenfels et al. 2008) under a microscope (Fig. S1). The processed nematodes were fixed in 70% ethanol and stored at − 20 °C. Total DNA extraction from the samples was performed using the Universal Genomic DNA Kit (Jiangsu CoWin Biotech Co., Jiangsu, China). Subsequently, the quality and concentration of the extracted DNA were assessed using Agilent5400.

Genome sequencing and data assembly

DNA samples were sent to Shenzhen Huitong Biotechnology Co., Ltd. (Shenzhen, China), for sequencing using the Illumina NovaSeq 6000 platform. The raw reads obtained from sequencing were filtered to generate clean reads, which were saved in FASTQ format. Sequencing produced a total of 12.65 Gb of filtered, clean data, which was assembled into contigs using SPAdes v3.14.1 (Bankevich et al. 2012). The read coverage depth map is depicted in Figure S2. These contigs were further extended and merged using PRICE and MITObim, resulting in the complete mitochondrial genome sequence (Hahn et al. 2013).

Gene annotation

The assembled mt genome sequence was initially compared with other strongylid nematodes via the BLAST online platform on NCBI to confirm its overall reliability. Subsequently, the complete mt genome sequence was annotated using the MITOS online tool (http://mitos.bioinf.uni-leipzig.de/index.py) (Bernt et al. 2013). After removing redundant annotations, manual curation was performed to define the start and stop codon positions of protein-coding genes. The MITOS tool was also employed to annotate tRNA and rRNA genes, identify the number of tRNAs, and predict their secondary structures. Finally, all curated gene annotations were re-validated through an additional BLAST comparison to ensure accuracy. The complete mt genome sequence of C. coronatus was deposited in the GenBank database under accession number OR834861.

Base composition, codon usage, amino acid composition of protein-coding genes, and relative synonymous codon usage (RSCU) were analyzed using MEGA5.0 (Tamura et al. 2011). Additionally, pairwise genetic distances among the mitochondrial genomes of 24 strongylid nematode species were calculated based on the Kimura 2-parameter model using the same software. Nucleotide bias was assessed using the formulas: AT-skew = (A—T) / (A + T) and GC-skew = (G—C) / (G + C).

Phylogenetic analysis

This study conducted phylogenetic analyses using maximum likelihood (ML) and Bayesian inference (BI) methods. The dataset comprised concatenated nucleotide sequences of 12 protein-coding genes from 23 strongylid nematode species currently available in GenBank, with Ancylostoma tubaeforme (accession no.: NC_034289) designated as the outgroup. The optimal substitution model (GTR + F + R4) was automatically selected using ModelFinder (Kalyaanamoorthy et al. 2017) implemented within the PhyloSuite software package (Zhang et al. 2020). The ML tree was constructed using IQ-TREE (Nguyen et al. 2015), and branch support was assessed with 5000 ultra-fast bootstrap replicates. BI analysis was conducted using MrBayes 3.2.6 (Huelsenbeck and Ronquist 2001). Posterior probabilities were estimated using Markov Chain Monte Carlo (MCMC) simulations, running for 2 million generations with sampling every 1000 generations. The first 25% of samples were discarded as burn-in. The resulting phylogenetic trees were visualized and edited using FigTree v1.4.4.

Results

Mt genome of Coronocyclus coronatus

Mt genome structure and characteristics

The mt genome of Coronocyclus coronatus is 13,870 bp in length, adopting a typical circular double-stranded DNA structure (Fig. 1). The base composition is A = 29.75%, T = 45.00%, C = 7.58%, G = 17.67%, with an AT content of 74.75% and a GC content of 25.25%. The AT-skew and GC-skew values were calculated as -0.204 and 0.399, respectively. This genome encodes 36 genes, comprising 12 protein-coding genes, 22 tRNA genes, 2 rRNA genes, and 2 non-coding regions. It lacks the atp8 gene. All genes are arranged in the GA3-type pattern and encoded on the positive strand. The genes in C. coronatus are closely arranged, and contained 18 intergenic regions and 4 gene overlaps, with no evidence of genomic rearrangements (Table 1).

Fig. 1.

Fig. 1

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Organization of the complete mt genome of Coronocyclus coronatus

Table 1.

Annotation of the mt genome of Coronocyclus coronatus

Genes/regions Start End Length Strand Intergenic nucleotides Number of aaa Initiation and stop codons Anticodon
ND1 1 873 873  +  0 290 TTG/TAG
ATP6 857 1480 624  +  -17 199 ATT/TAA
tRNA-Lys (K) 1492 1553 62  +  11 TTT
tRNA-LeuTTA (L2) 1588 1655 68  +  34 TAA
tRNA-SerAGA (S1) 1643 1695 53  +  -13 TCT
ND2 1696 2541 846  +  0 281 TTG/TAA
tRNA-Ile (I) 2551 2610 60  +  9 GAT
tRNA-Arg (R) 2637 2691 55  +  26 ACG
tRNA-Gln (Q) 2707 2761 55  +  15 TTG
tRNA-Phe (F) 2768 2824 57  +  6 GAA
CYTB 2825 3937 1113  +  0 370 ATT/TAA
tRNA-LeuCTA (L1) 3952 4006 55  +  14 TAG
COX3 4007 4772 766  +  0 255 ATT/T
tRNA-Phe (T) 4773 4828 56  +  0 TGT
ND4 4856 6058 1203  +  27 400 ATA/TAA
AT-region 6059 6140 82  +  0
COX1 6141 7718 1578  +  0 525 ATT/TAG
tRNA-Cys (C) 7723 7777 55  +  4 GCA
tRNA-Met (M) 7796 7854 59  +  18 CAT
tRNA-Asp (D) 7862 7922 61  +  7 GTC
tRNA-Gly (G) 7930 7985 56  +  7 TCC
COX2 7986 8681 696  +  0 231 ATT/TAA
tRNA-His (H) 8681 8735 55  +  -1 GTG
rrnL 8736 9710 975  +  0
ND3 9711 10046 336  +  0 111 ATT/TAA
ND5 10055 11638 1584  +  8 527 ATT/TAG
tRNA-Ala (A) 11642 11698 57  +  3 TGC
AT-region 11699 11971 273  +  0
tRNA-Pro (P) 11972 12026 55  +  0 TGG
tRNA-Val (V) 12061 12114 54  +  34 TAC
ND6 12115 12549 435  +  0 144 ATT/TAA
ND4L 12606 12839 234  +  56 77 ATT/TAG
tRNA-Trp (W) 12868 12924 57  +  28 TCA
tRNA-Glu (E) 12,943 13002 60  +  18 TTC
rrnS 13003 13702 700  +  0
tRNA-SerTCA (S2) 13703 13759 57  +  0 TGA
tRNA-Asn (N) 13759 13815 57  +  -1 GTT
tRNA-Tyr (Y) 13816 13870 55  +  0 GTA
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Protein-coding genes and relative synonymous codon usage (RSCU)

The 12 protein-coding genes of C. coronatus comprised a total of 10,264 bp; nine of them (ATP6, CYTB, COX3, COX1, COX2, ND3, ND5, ND6, ND4L) used ATT as the initiation codon; ND1 and ND2 used TTG; and ND4 used ATA. Most genes terminate with standard termination codons: TAA (ATP6, ND2, CYTB, ND4, COX2, ND3, ND6) and TAG (ND1, COX1, ND5, ND4L). Notably, the gene coding for COX3 has an incomplete termination codon "T". The overall A + T content of the protein-coding genes was 73.05%, with AT-skew and GC-skew values of -0.267 and 0.393, respectively, indicating marked AT bias (Table 1).

In the absence of termination codons, the 12 protein-coding genes within the C. coronatus mt genome collectively encode 3,410 amino acids. Among the 26 preferred codons (RSCU > 1) (Fig. 2), the most frequently used codon was UUU (Phe), with 425 occurrences and an RSCU of 1.94. This was followed by UUA (Leu) with 305 occurrences and AUU (Ile) with 232 occurrences, exhibiting RSCU values of 3.52 and 1.91, respectively. The codons exhibiting the lowest usage frequency were CUC (Leu), CGC (Arg), and UGC (Cys), with occurrence counts of 0, 0, and 2, and corresponding RSCU values of 0.00, 0.00, and 0.11 (Table S1).

Fig. 2.

Fig. 2

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The synonymous codon usage frequency of the 12 protein-coding genes of the Coronocyclus coronatus

Based on the concatenated nucleotide sequences of the 12 protein-coding genes, the pairwise genetic distances among the 24 strongylid nematode species were calculated, ranging from 0.059 to 0.201 (Table S2). The maximum genetic distance was observed between Strongylus vulgaris and Cylicodontophorus bicoronatus, while the minimum was found between Cyathostomum pateratum and Cyathostomum catinatum. Notably, the relatively small genetic distance between C. coronatus and Cyclicostephanus calicatus indicates a close phylogenetic relationship between these two species.

Mt genome tRNA, rRNA and non-coding regions

The total length of the 22 tRNA sequences was determined to be 1,259 bp, with lengths ranging from 53 to 68 bp and an A + T content of 77.8%. Except for trnL2, which exhibits a cloverleaf-like structure, the secondary structures of the remaining 21 tRNAs exhibited atypical clover-leaf structures. Among them, two trnS genes lacked the DHU arm and DHU loop. The trnK and trnM genes lacked the TΨC-arm but retained the TΨC-loop. The other 17 tRNA genes lacked the TΨC-arm and TΨC-loop, substituted by the TVreplacement loop. Additionally, all tRNA genes except trnR and trnW exhibited base mismatches, including 48 G-U mismatches as well as one each of A-G, A-A, and U-U mismatches.

The two rRNAs are characterized as follows: the 16S rRNA (975 bp), located between trnH and ND3, has an A + T content of 82.2%; The 12S rRNA (700 bp), positioned between the non-protein coding gene trnE and trnS2, shows an A + T content of 75.9%. Two non-coding regions were identified in the mt genome of C. coronatus. One is located between ND4 and COX1, is 82 bp long, and has an A + T content of 76.8%. The other, located between trnA and trnP, is 273 bp long with an A + T content of 85.7%. Both regions are AT-rich.

Phylogenetic analysis of strongylid nematodes

Based on the 12 protein-coding genes of the mt genome, with A. tubaeforme as the outgroup, phylogenetic trees of 24 species of strongylid nematodes were constructed using Maximum Likelihood (ML) and Bayesian Inference (BI) methods (Fig. 3). The topologies derived from both analyses were congruent, differing only in nodal support values. Phylogenetic reconstruction recovered strongylid nematodes into two major groups, one group containing species of the genus Strongylus (subfamily Strongylinae), and the other group containing all species of subfamily Cyathostominae and species of the genus Triodontophorus (subfamily Strongylinae). Within the Cyathostominae group, C. coronatus shares a closer phylogenetic relationship with C. calicatus than with its congeners (Coronocyclus labiatus and Coronocyclus labratus). As shown in Fig. 3, C. coronatus and C. calicatus form a highly supported clade (support values: of 1.00/100), which is sister to the genus Cylicocyclus.

Fig. 3.

Fig. 3

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Phylogenetic tree of 24 nematodes in Strongylidae based on concatenated amino acid sequences of 12 protein coding genes analyzed by maximum likelihood (ML) and Bayesian inference (BI) using Ancylostoma tubaeforme as an outgroup. Statistical support values (Bootstrap/posterior probability) of ML/BI analysis are shown above the nodes

Discussion

The complete mt genome of Coronocyclus coronatus is described for the first time in this study. The length of this mt genome is comparable to that of most nematodes belonging to the subclass Secernentia, such as Cylicocyclus radiatus (Hu et al. 2020), Cylicocyclus ultrajectinus (Hao et al. 2024), Cyathostomum tetracanthus (Wang et al. 2020), and Cylicostephanus longibursatus (Ma et al. 2024). However, it is significantly shorter than those of Adenophorea nematodes, exemplified by Romanomermis culicivorax (Azevedo and Hyman 1993), and Steinernema litorale (Kikuchi et al. 2016). The mt genome of C. coronatus is compact and highly conserved, encoding a total of 36 genes. This characteristic is identical to that reported for strongylid nematodes (Stein et al. 2003; Hu et al. 2020; Gao et al. 2021). Its genome contains two AT-rich non-coding regions, whereas the mitochondrial genome of Triodontophorus brevicauda contains three non-coding regions (Gao et al. 2017). Notably, compared to adenophorean nematodes, this genome lacks the ATP8 gene (Lavrov and Brown 2001; Mohandas et al. 2014). The gene arrangement pattern is consistent with other Strongylidae nematodes, being of the GA3-type, which is a common arrangement pattern among animal-parasitic nematodes (Liu et al. 2013; Gao et al. 2017). All genes are encoded on the same strand, with overlaps and intergenic spacers present between genes. No gene rearrangements were detected.

In the 12 protein-coding genes of C. coronatus, the usage of start and stop codons resembles that observed in most animal-parasitic nematodes, such as Haemonchus contortus, Ascaris ovis, and Gnathostoma nipponicum (Jex et al. 2008; Sun et al. 2017; Chen et al. 2021). A notable exception is the COX3 gene, which consistently uses an incomplete "T" as its stop signal. Comparative analysis reveals that the COX3 genes of all reported strongylid nematodes also utilize 'T' as the stop codon (Xu et al. 2015; Hu et al. 2020; Ma et al. 2024), with the complete stop codon formed through 3’ polyadenylation during post-transcriptional processing. The AT base bias is evident not only in nucleotide composition but also in codon usage. Among the 26 preferred codons (RSCU > 1) encoding amino acids, the frequency of AT bases at the third codon position is higher than that of GC bases, consistent with previously reported codon usage patterns in strongylid nematodes (Hu et al. 2020; Gao et al. 2021). Throughout species evolution, gene mutation and selection mechanisms play a crucial role in shaping codon usage bias. Research on codon bias is therefore significant for elucidating the transmission patterns of genetic information and advancing studies on species origin and evolution (Bohonak and Jenkins 2003).

The structural characteristics of the 22 tRNA genes share similarities with the tRNA structural patterns observed in the Trichinella mt genome. A difference is that Trichinella retains eight tRNA genes exhibiting the typical cloverleaf secondary structure (Lavrov and Brown 2001). The sequences of the two rRNA subunits show limited variation in length, and their positional distribution resembles that found in nematodes within the same family and order (Duan et al. 2015; Xu et al. 2015). This distribution differs from the gene locations reported in Trichuris ovis, Trichuris discolor, Trichinella spp., and Spirocerca lupi (Lavrov and Brown 2001; Liu et al. 2012, 2013). This variation may be associated with differences in gene arrangement patterns among the aforementioned species.

The mt genome sequence of C. coronatus contains two highly variable AT-rich regions, consistent with findings in Coronocyclus labiatus, Cylicodontophorus bicoronatus, C. radiatus, and Cylicocyclus auriculatus (Hu et al. 2020; Gao et al. 2021). Among animal-parasitic nematodes, the number of non-coding regions is not fixed. Parascaris equorum and Bunostomum phlebotomum possess only a single non-coding region, whereas Strongylus equinus and Triodontophorus brevicauda harbor three non-coding regions (Gao et al. 2014; Duan et al. 2015; Xu et al. 2015). The two non-coding regions in C. coronatus differ in size, with the longer one being 273 bp and the shorter one being 82 bp. Studies have indicated that mt genome size is correlated with the length and number of non-coding regions (Yatawara et al. 2010).

Phylogenetic analysis revealed that the 24 species of strongylid nematodes formed two major groups. The genus Triodontophorus (subfamily Strongylinae) clustered with the subfamily Cyathostominae as sister groups within a large clade, rather than grouping with the genus Strongylus (subfamily Strongylinae). This result conflicts with the traditional morphology-based classification by Lichtenfels et al. (2008), but is consistent with conclusions derived from studies utilizing complete mitochondrial genomes as molecular markers to investigate the taxonomic status of nematodes such as S. equinus, C. radiatus, and C. bicoronatus (Duan et al. 2015; Xu et al. 2015; Wang et al. 2020; Gao et al. 2021). This also indicates that classification based solely on morphological characteristics may not accurately reflect the true taxonomic position of nematodes. C. coronatus did not form a monophyletic group with other Coronocyclus species. Instead, it first clustered with Cylicostephanus calicatus to form a small subclade, which then grouped as a sister clade to the genus Cylicocyclus. This finding aligns with phylogenetic analyses by Bredtmann et al. (2019) based on ITS-2 genes, Louro et al. (2021) based on ITS-2 and COI genes, and by Hung et al. (2000) based on ITS-1 and ITS-2 sequences, all of which showed C. coronatus and C. calicatus clustering within the same group, indicating a close phylogenetic relationship between these two species. Mt genomes contain more comprehensive genetic information and allow for a more precise elucidation of evolutionary history and taxonomic status. This approach clearly produces different results compared to traditional morphological classification. Therefore, the taxonomic position of C. coronatus requires reassessment, and the classification of horse strongyle taxa warrants redefinition.

Conclusion

This study presents the first complete mitochondrial genome sequence of Coronocyclus coronatus, which is 13,870 bp in length. The circular genome contains 12 protein-coding genes (PCGs), 22 tRNAs, 2 rRNAs, and 2 non-coding regions. All genes are encoded on the same strand and exhibit a significant AT bias (74.75%). Phylogenetic analysis based on the 12 PCGs revealed that C. coronatus is more closely related to Cylicocyclus than to other Coronocyclus species. These results provide key molecular markers for the identification of this species and offer valuable data for future research in population genetics and evolutionary biology.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PNG 2735 KB) (2.7MB, png)
Supplementary file2 (JPG 1469 KB) (1.4MB, jpg)
Supplementary file3 (DOCX 19 KB) (19.4KB, docx)
Supplementary file4 (DOCX 28 KB) (28.2KB, docx)

Author contributions

Yan Hao: Writing—review & editing, Writing—original draft, Methodology, Investigation, Data curation, Conceptualization. Yinghao Xia: Writing—review & editing, Writing—original draft, Methodology, Data curation, Conceptualization. Liqun Ma: Writing—review & editing, Writing—original draft, Methodology, Investigation, Data curation, Conceptualization. Zhe Hao: Writing—review & editing, Writing—original draft, Methodology, Data curation, Conceptualization. Bing LI: Writing—review & editing, Writing—original draft, Methodology, Investigation, Data curation,. Yanzhen Bu: review, Methodology, Investigation, Data curation, Conceptualization.

Funding

This work was supported by a major project of National Natural Science Foundation of China (No. 31372163) and the Research Grants from the Science and Technology Department of Henan Province, China (Nos. 142102310121, 192102310518, 242102311238).

Data availability

The genome sequence data that support the findings of this study are openly available in GenBank of NCBI at https://www.ncbi.nlm.nih.gov, under the accession number OR834861.

Declarations

Ethics approval

Not applicable.

Consent to participate and consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Footnotes

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary file1 (PNG 2735 KB) (2.7MB, png)
Supplementary file2 (JPG 1469 KB) (1.4MB, jpg)
Supplementary file3 (DOCX 19 KB) (19.4KB, docx)
Supplementary file4 (DOCX 28 KB) (28.2KB, docx)

Data Availability Statement

The genome sequence data that support the findings of this study are openly available in GenBank of NCBI at https://www.ncbi.nlm.nih.gov, under the accession number OR834861.

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