Chromosome-scale nuclear genome and proteome of Anoplocephala perfoliata elucidate lineage-specific features of a ‘neglected’ equine tapeworm.
Abstract: is the most prevalent and pathogenic tapeworm (cestode) of horses worldwide, yet it remains molecularly understudied. Here, we present the mitochondrial and chromosome-scale nuclear genomes and matched somatic proteome for this parasite, establishing the first high-resolution molecular resource for the family Anoplocephalidae. This parasite was first characterised morphologically and then by its mitochondrial genome (size: 13,776 bp). Its complete nuclear genome (size: 372.3 Mb) was assembled and characterised; it encodes 9,711 protein-coding genes, 78.2% of which were functionally annotated and ~ 80% supported by transcriptomic evidence. Proteomic analysis confirmed 758 proteins in previously-analysed excretory/secretory (ES) products from adult worms, including highly expressed components of the ubiquitin–proteasome system, stress response families – e.g., translationally controlled tumour proteins (TCTPs) and universal stress proteins (USPs) – and cytoskeletal scaffolds. Approximately 6.5% of the genome contains retroelements, predominantly LINEs. Comparative genomic analyses revealed a relatively conserved synteny with members of the family Taeniidae (, and ) and a pronounced structural divergence from (Hymenolepididae), reflecting mosaic genome evolution within the order Cyclophyllidea. Classification of proteins inferred from the genome identified GTPases, kinases, peptidases and secretome-associated proteins among the most abundant groups. A subset of proteins exhibited signal peptides or extracellular localisation, suggesting their role as parasite-derived proteins (PDPs) involved in host–parasite communication and immune evasion. This integrated genomic and proteomic framework reveals lineage-specific molecular adaptations in and provides a foundation for future functional and translational investigations of this and closely related cestodes. The online version contains supplementary material available at 10.1186/s12864-026-12554-9.
Publication Date: 2026-01-21 PubMed ID: 41566420PubMed Central: PMC12908361DOI: 10.1186/s12864-026-12554-9Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
Cite This Article
APA
Young ND, Wang T, Ang CS, Lale D, Fuehrer HP, Sumanam SB, Korhonen PK, Chang BCH, Gasser RB.
(2026).
Chromosome-scale nuclear genome and proteome of Anoplocephala perfoliata elucidate lineage-specific features of a ‘neglected’ equine tapeworm.
BMC Genomics, 27(1), 201.
https://doi.org/10.1186/s12864-026-12554-9 Publication
Researcher Affiliations
- Department of Veterinary Biosciences, Melbourne Veterinary School, The University of Melbourne, Parkville, VIC, 3010, Australia. nyoung@unimelb.edu.au.
- Department of Veterinary Biosciences, Melbourne Veterinary School, The University of Melbourne, Parkville, VIC, 3010, Australia.
- Bio21 Mass Spectrometry and Proteomics Facility, The University of Melbourne, Parkville, VIC, 3010, Australia.
- University Equine Hospital, Clinical Unit of Equine Internal Medicine, University of Veterinary Medicine Vienna, Vienna, Austria.
- Institute of Virology, Vetsuisse Faculty, University of Zurich, Zurich, Switzerland.
- Institute of Parasitology, University of Veterinary Medicine Vienna, Vienna, 1210, Austria.
- Department of Veterinary Biosciences, Melbourne Veterinary School, The University of Melbourne, Parkville, VIC, 3010, Australia.
- Department of Veterinary Biosciences, Melbourne Veterinary School, The University of Melbourne, Parkville, VIC, 3010, Australia.
- Department of Veterinary Biosciences, Melbourne Veterinary School, The University of Melbourne, Parkville, VIC, 3010, Australia.
- Department of Veterinary Biosciences, Melbourne Veterinary School, The University of Melbourne, Parkville, VIC, 3010, Australia. robinbg@unimelb.edu.au.
Grant Funding
- FT230100559 / Australian Research Council
- LP180101085 / Australian Research Council
Conflict of Interest Statement
Declarations. Ethics approval and consent to participate: Not applicable. Consent for publication: Not applicable. Competing interests: The authors declare no competing interests.
References
This article includes 62 references
- Beveridge I, Family Anoplocephalidae Cholodkovsky, 1902. In: Khalil LF, Jones A, Bray RA, editors. Keys to the cestode parasites of vertebrates. Wallingford: CAB International; 1994. pp. 315–366. ISBN 0851988792.
- Caira JN, Jensen K. Planetary biodiversity inventory (2008–2017): Tapeworms from vertebrate bowels of the Earth. The University of Kansas, Natural History Museum, Special Publication No. 25. 2017. pp 1-463. ISBN 9780998857803.
- Geary TG. New paradigms in research on . Parasites Vectors. 2023;16:247.n
- Olson PD, Zarowiecki M, Kiss F, Brehm K. Cestode genomics – progress and prospects for advancing basic and applied aspects of flatworm biology. Parasite Immunol. 2012;34:130–50.
- Tsai IJ, Zarowiecki M, Holroyd N, Garciarrubio A, Sánchez-Flores A, Brooks KL, Tracey A, Bobes RJ, Fragoso G, Sciutto E, Aslett M, Beasley H, Bennett HM, Cai X, Camicia F, Clark R, Cucher M, De Silva N, Day TA, Deplazes P, Estrada K, Fernández C, Holland PWH, Hou J, Hu S, Huckvale T, Hung SS, Kamenetzky L, Keane JA, Kiss F, Koziol U, Lambert O, Liu K, Luo X, Luo Y, Macchiaroli N, Nichol S, Paps J, Parkinson J, Pouchkina-Stantcheva N, Riddiford N, Rosenzvit M, Salinas G, Wasmuth JD, Zamanian M, Zheng Y, Taenia solium Genome Consortium, Cai J, Soberón X, Olson PD, Laclette JP, Brehm K, Berriman M. The genomes of four tapeworm species reveal adaptations to parasitism. Nature. 2013;496:57–63.
- Zheng H, Zhang W, Zhang L, Zhang Z, Li J, Lu G, Zhu Y, Wang Y, Huang Y, Liu J, Kang H, Chen J, Wang L, Chen A, Yu S, Gao Z, Jin L, Gu W, Wang Z, Zhao L, Shi B, Wen H, Lin R, Jones MK, Brejova B, Vinar T, Zhao G, McManus DP, Chen Z, Zhou Y, Wang S. The genome of the hydatid tapeworm . Nat Genet. 2013;45:1168–75.n
- Li W, Liu B, Yang Y, Ren Y, Wang S, Liu C, Zhang N, Qu Z, Yang W, Zhang Y, Yan H, Jiang F, Li L, Li S, Jia W, Yin H, Cai X, Liu T, McManus DP, Fan W, Fu B. The genome of tapeworm sheds light on Understanding parasitic mechanism and control of coenurosis disease. DNA Res. 2018;25:499–510.n
- International Helminth Genomes Consortium. Comparative genomics of the major parasitic worms. Nat Genet. 2019;51:163–74.
- Williamson RMC, Gasser RB, Middleton D, Beveridge I. The distribution of in the intestine of the horse and associated pathological changes. Vet Parasitol. 1997;73:225–41.n
- Gasser RB, Williamson RMC, Beveridge I. of horses—significant scope for further research, improved diagnosis and control. Parasitology. 2005;131:1–13.n
- Riddiford N, Olson PD. Wnt gene loss in flatworms: taxonomic and phylogenetic implications. Evol Dev. 2011;13:176–87.
- Thompson RCA, Lymbery AJ. Let’s not forget the thinkers: the legacy of Desmond Smyth and fundamental questions in parasite biology. Trends Parasitol. 2013;29:581–4.
- Koziol U, Brehm K. Recent advances in genomics and stem cell research. Vet Parasitol. 2015;213:92–102.n
- Koziol U. Evolutionary developmental biology of tapeworms: recent progress and future perspectives. EvoDevo. 2017;8:12.
- Hewitson JP, Grainger JR, Maizels RM. Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Mol Biochem Parasitol. 2009;167:1–11.
- Guo A. The complete mitochondrial genome of , the first representative for the family anoplocephalidae. Parasites Vectors. 2015;8:549.n
- Guo A. Complete mitochondrial genome of solidifying the species. Korean J Parasitol. 2016;54:369–73.n
- Seppey M, Manni M, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness. Methods Mol Biol. 2019;1962:227–45.
- Korhonen PK, Kinkar L, Young ND, Cai H, Lightowlers MW, Gauci C, Jabbar A, Chang BCH, Wang T, Hofmann A, Koehler AV, Li J, Li J, Wang D, Yin J, Yang H, Jenkins DJ, Saarma U, Laurimäe T, Rostami-Nejad M, Irshadullah M, Mirhendi H, Sharbatkhori M, Ponce-Gordo F, Simsek S, Casulli A, Zait H, Atoyan H, de la Rue ML, Romig T, Wassermann M, Aghayan SA, Gevorgyan H, Yang B, Gasser RB. Chromosome-scale (genotype G1) genome reveals the Eg95 gene family and conservation of the EG95-vaccine molecule. Commun Biol. 2022;5:199.n
- Olson PD, Zarowiecki M, James K, Baillie A, Bartl G, Burchell P, Chellappoo A, Jarero F, Tan LY, Holroyd N, Berriman M. Genome-wide transcriptome profiling and Spatial expression analyses identify signals and switches of development in tapeworms. EvoDevo. 2018;9:21.
- Olson PD, Tracey A, Baillie A, James K, Doyle SR, Buddenborg SK, Rodgers FH, Holroyd N, Berriman M. Complete representation of a tapeworm genome reveals chromosomes capped by centromeres, necessitating a dual role in segregation and protection. BMC Biol. 2020;18:165.
- Cunningham LJ, Olson PD. Description of (Nottingham strain): a classical tapeworm model for research in the genomic era. Parasites Vectors. 2010;3:123.n
- Hautala K, Pursiainen J, Näreaho A, Nyman T, Varmanen P, Sukura A, Nielsen MK, Savijoki K. Label-free quantitative proteomics and Immunoblotting identifies immunoreactive and other excretory-secretory (E/S) proteins of . Front Immunol. 2022;13:1045468.n
- Rogers M, Kmath S, McManus D, Jones M, Gordon C, Navarro S. excretory/secretory products: an untapped library of tolerogenic immunotherapeutics against food allergy. Clin Transl Immunol. 2024;13:e70007.
- Drurey C, Maizels RM. Helminth extracellular vesicles: interactions with the host immune system. Mol Immunol. 2021;137:124–33.
- Marcilla A, Trelis M, Cortés A, Sotillo J, Cantalapiedra F, Minguez MT, Valero ML, del Sánchez MM, Muñoz-Antolí C, Toledo R, Bernal D. Extracellular vesicles from parasitic helminths contain specific excretory/secretory proteins and are internalised in intestinal host cells. PLoS ONE. 2012;7:e45974.
- Cwiklinski K, de la Torre-Escudero E, Trelis M, Bernal D, Dufresne PJ, Brennan GP, O’Neill SM, Tort JF, Paterson S, Marcilla A, Dalton JP. The extracellular vesicles of the helminth pathogen : biogenesis, protein cargo and functional biology. Mol Cell Proteom. 2015;14:3258–73.
- Nowacki FC, Swain MT, Klychnikov OI, Niazi U, Ivens A, Quinnell RJ, Maizels RM, Hall R. Protein and small noncoding RNA-enriched extracellular vesicles are released by the pathogenic blood fluke . J Extracell Vesicles. 2015;4:28665.n
- Zheng H, Zhang W, Zhang L, Zhang Z, Li J, Lu G, Zhu Y, Wang Y, Liu J, Zhang B, Zhou Y, Zheng Y, Wang S, Yan X, Wang X, Yu S, Lin R, Zhao W, McManus DP, Wen H. Regulatory effects of extracellular vesicles on human monocytes and macrophages. Int J Parasitol. 2017;47:675–85.n
- Siles-Lucas M, Sánchez-Ovejero C, González-Sánchez M, González E, García MP, Zafra R, Pérez-Arellano JL, Martínez-Sernández V, Muñoz C, Gárate T. Extracellular vesicles from metacestodes: analysis of protein content and potential functions. PLoS Negl Trop Dis. 2018;12:e0007032.
- Liu F, Li X, Wang L, Zhao Y, Zhang Z, Hou J, Wen H, Craig PS, Giraudon P, Vuitton DA, Wang J. Proteomic profiling of serum extracellular vesicles identifies diagnostic markers for echinococcosis. PLoS Negl Trop Dis. 2022;16:e0010814.
- Siles-Lucas M, Morchón R, Simon F, Manzano-Román R. Cestode parasites release extracellular vesicles with microRNAs and immunodiagnostic protein cargo. Int J Parasitol. 2017;47:675–86.
- Penna-Gonçalves V, Willmott NJ, Kelly MBJ, Black JR, Lowe EC, Herberstein ME. Comparing MicroCT staining and scanning methodology for brain studies in various sizes of spiders. J Comp Neurol. 2025;533:e70017. 10.1002/cne.70017.
- Kahane Z. Anatomie von Göze, als Beitrag Zur Kenntnis der Zestoden. Z Wiss Zool. 1880;34:175–254.
- Spasskii AA. Anoplocephalate tapeworms of domestic and wild animals. In: Skrjabin KI, editor. . Vol. 1. Israel Program for Scientific Translations, Jerusalem (English translation, 1966); 1951. pp 1-783.ISBN 9780706505785.
- Kolmogorov M, Yuan J, Lin Y, Pevzner PA. Assembly of long, error-prone reads using repeat graphs. Nat Methods. 2019;16:753–60.
- Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. 2018;34:3094–100.
- Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. The sequence alignment/map format and samtools. Bioinformatics. 2009;25:2078–9.
- Bernt M, Donath A, Jühling F, Externbrink F, Florentz C, Fritzsch G, Pütz J, Middendorf M, Stadler PF. MITOS: improved de novo metazoan mitochondrial genome annotation. Mol Phylogenet Evol. 2013;69:313–9.
- Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–9.
- Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61:539–42.
- Cheng H, Concepcion GT, Feng X, Zhang H, Li H. Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm. Nat Methods. 2021;18:170–5.
- Roach MJ, Schmidt SA, Borneman AR. Purge haplotigs: allelic contig reassignment for third-gen diploid genome assemblies. BMC Bioinformatics. 2018;19:460.
- Zhang H, Song L, Wang X, Cheng H, Wang C, Meyer CA, Liu T, Tang M, Aluru S, Yue F, Liu XS, Li H. Fast alignment and preprocessing of chromatin profiles with chromap. Nat Commun. 2021;12:6566.
- Zhou C, McCarthy SA, Durbin R. YaHS: yet another Hi-C scaffolding tool. Bioinformatics. 2023;39:btac808.
- Durand NC, Shamim MS, Machol I, Rao SSP, Huntley MH, Lander ES, Aiden EL. Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Syst. 2016;3:95–8.
- Serizay J, Matthey-Doret C, Bignaud A, Baudry L, Koszul R. Orchestrating chromosome conformation capture analysis with bioconductor. Nat Commun. 2024;15:1072.
- Ludwig A, Pippel M, Myers G, Hiller M. DENTIST – using long reads for closing assembly gaps at high accuracy. Gigascience. 2022;11:giab100.
- Flynn JM, Hubley R, Goubert C, Rosen J, Clark AG, Feschotte C, Smit AFA. RepeatModeler2 for automated genomic discovery of transposable element families. Proc Natl Acad Sci U S A. 2020;117:9451–7.
- Turnbull R, Young ND, Tescari E, Skerratt LF, Kosch TA. Terrier: a deep learning repeat classifier. Brief Bioinform. 2025;26:bbaf442.
- Tarailo-Graovac M, Chen N. Using RepeatMasker to identify repetitive elements in genomic sequences. Curr Protoc Bioinform. 2009;4:4.10.1–4.10.14.
- Hoff KJ, Lomsadze A, Borodovsky M, Stanke M. Whole-genome annotation with BRAKER. Methods Mol Biol. 2019;1962:65–95.
- Brůna T, Hoff KJ, Lomsadze A, Stanke M, Borodovsky M. BRAKER2: automatic eukaryotic genome annotation with GeneMark-EP + and AUGUSTUS supported by a protein database. NAR Genom Bioinform. 2021;3:lqaa108.
- Keilwagen J, Hartung F, Paulini M, Twardziok SO, Grau J. Combining RNA-seq data and homology-based gene prediction for plants, animals and fungi. BMC Bioinformatics. 2018;19:189.
- Keilwagen J, Hartung F, Grau J. GeMoMa: homology-based gene prediction utilizing intron position conservation and RNA-seq data. Methods Mol Biol. 2019;1962:161–77.
- UniProt Consortium. UniProt: the universal protein knowledgebase in 2023. Nucleic Acids Res. 2023;51:D523–31.
- Nevers Y, Warwick Vesztrocy A, Rossier V, Train C-M, Altenhoff A, Dessimoz C, Glover NM. OMark: quality assessment of gene repertoire annotations. Nat Biotechnol. 2025;43:124–33.
- Cantalapiedra CP, Hernández-Plaza A, Letunic I, Bork P, Huerta-Cepas J. eggNOG-mapper v2: functional annotation, orthology assignments and domain prediction at the metagenomic scale. Mol Biol Evol. 2021;38:5825–9.
- Emms DM, Kelly S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 2015;16:157.
- Lovell JT, Sreedasyam A, Schranz ME, Wilson M, Carlson JW, Harkess A, Emms D, Goodstein DM, Schmutz J. GENESPACE tracks regions of interest and gene copy number variation across multiple genomes. eLife. 2022;11:e78526.
- Tyanova S, Temu T, Cox J. The MaxQuant computational platform for mass spectrometry-based shotgun proteomics. Nat Protoc. 2016;11:2301–19.
- Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res. 2016;44:D457–62.
Citations
This article has been cited 0 times.Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists