Section: Genomics
Topic: Evolution, Genetics/genomics

The genome sequence of the Montseny horsehair worm, Gordionus montsenyensis sp. nov., a key resource to investigate Ecdysozoa evolution

10.24072/pcjournal.381 - Peer Community Journal, Volume 4 (2024), article no. e32.

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Nematomorpha, also known as Gordiacea or Gordian worms, are a phylum of parasitic organisms that belong to the Ecdysozoa, a clade of invertebrate animals characterized by molting. They are one of the less scientifically studied animal phyla, and many aspects of their biology and evolution are still unknown, partially due to the lack of genomic resources for this phylum. As part of the European Reference Genome Atlas pilot effort to generate reference genomes for European biodiversity, we present the taxonomic description and chromosome-level genome assembly of a newly described species of Nematomorpha (Gordionus montsenyensis Schmidt-Rhaesa & Fernández sp. nov.). The final assembly has a total length of 288 Mb in 396 scaffolds with an N50 of 64.4 Mb, 97% of which is scaffolded into 5 pseudochromosomes. The circular mitochondrial genome was also assembled into a 15-kilobases sequence. Gene annotation predicted 10,320 protein-coding genes in the nuclear genome. In this study, we contribute a key genomic resource to not only explore the evolution of Ecdysozoa, but also to further our understanding on the genomic basis of parasitic lifestyles. In addition, we describe a species new to science from this enigmatic animal phyla.

Published online:
DOI: 10.24072/pcjournal.381
Type: Research article
Keywords: Nematomorpha, Gordian worms, reference genome
Eleftheriadi, Klara 1; Guiglielmoni, Nadège 2; Salces-Ortiz, Judit 1; Vargas-Chavez, Carlos 1; Martínez-Redondo, Gemma I. 1; Gut, Marta 3; Flot, Jean-François 4, 5; Schmidt-Rhaesa, Andreas 6; Fernández, Rosa 1

1 Metazoa Phylogenomics Lab, Biodiversity Program, Institute of Evolutionary Biology (CSIC-Universitat Pompeu Fabra), Passeig marítim de la Barceloneta 37-49, 08003 Barcelona, Spain
2 Universität zu Köln, Institut für Zoologie, Zülpicher str. 47b, Cologne, Germany
3 Centro Nacional de Análisis Genómico (CNAG), C/Baldiri Reixac 4, 08028 Barcelona, Spain
4 Evolutionary Biology and Ecology, Department of Organismal Biology, Université libre de Bruxelles (ULB), Av. F.D. Roosevelt 50, 1050, Brussels, Belgium
5 Interuniversity Institute of Bioinformatics in Brussels – (IB)², Brussels, Belgium
6 Centre for Taxonomy and Morphology, Leibniz Institute for the Analysis of Biodiversity Change, Martin-Luther-King-Platz 3, 20146 Hamburg, Germany
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
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     author = {Eleftheriadi, Klara and Guiglielmoni, Nad\`ege and Salces-Ortiz, Judit and Vargas-Chavez, Carlos and Mart{\'\i}nez-Redondo, Gemma I. and Gut, Marta and Flot, Jean-Fran\c{c}ois and Schmidt-Rhaesa, Andreas and Fern\'andez, Rosa},
     title = {The genome sequence of the {Montseny} horsehair worm, {\protect\emph{Gordionus} montsenyensis} sp. nov., a key resource to investigate {Ecdysozoa} evolution},
     journal = {Peer Community Journal},
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Eleftheriadi, Klara; Guiglielmoni, Nadège; Salces-Ortiz, Judit; Vargas-Chavez, Carlos; Martínez-Redondo, Gemma I.; Gut, Marta; Flot, Jean-François; Schmidt-Rhaesa, Andreas; Fernández, Rosa. The genome sequence of the Montseny horsehair worm, Gordionus montsenyensis sp. nov., a key resource to investigate Ecdysozoa evolution. Peer Community Journal, Volume 4 (2024), article  no. e32. doi : 10.24072/pcjournal.381. https://peercommunityjournal.org/articles/10.24072/pcjournal.381/

Peer reviewed and recommended by PCI : 10.24072/pci.genomics.100252

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Aguinaldo, A. M. A.; Turbeville, J. M.; Linford, L. S.; Rivera, M. C.; Garey, J. R.; Raff, R. A.; Lake, J. A. Evidence for a clade of nematodes, arthropods and other moulting animals, Nature, Volume 387 (1997) no. 6632, pp. 489-493 | DOI

[2] Baudry, L.; Guiglielmoni, N.; Marie-Nelly, H.; Cormier, A.; Marbouty, M.; Avia, K.; Mie, Y. L.; Godfroy, O.; Sterck, L.; Cock, J. M.; Zimmer, C.; Coelho, S. M.; Koszul, R. instaGRAAL: chromosome-level quality scaffolding of genomes using a proximity ligation-based scaffolder, Genome Biology, Volume 21 (2020) no. 1 | DOI

[3] Begay, A. C.; Schmidt-Rhaesa, A.; Bolek, M. G.; Hanelt, B. Two new Gordionus species (Nematomorpha: Gordiida) from the southern Rocky Mountains (USA), Zootaxa, Volume 3406 (2012) no. 1 | DOI

[4] Blaxter, M. L.; De Ley, P.; Garey, J. R.; Liu, L. X.; Scheldeman, P.; Vierstraete, A.; Vanfleteren, J. R.; Mackey, L. Y.; Dorris, M.; Frisse, L. M.; Vida, J. T.; Thomas, W. K. A molecular evolutionary framework for the phylum Nematoda, Nature, Volume 392 (1998) no. 6671, pp. 71-75 | DOI

[5] Bolger, A. M.; Lohse, M.; Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data, Bioinformatics, Volume 30 (2014) no. 15, pp. 2114-2120 | DOI

[6] Brůna, T.; Hoff, K. J.; Lomsadze, A.; Stanke, M.; Borodovsky, M. BRAKER2: automatic eukaryotic genome annotation with GeneMark-EP+ and AUGUSTUS supported by a protein database, NAR Genomics and Bioinformatics, Volume 3 (2021) no. 1 | DOI

[7] Brůna, T.; Lomsadze, A.; Borodovsky, M. GeneMark-EP+: eukaryotic gene prediction with self-training in the space of genes and proteins, NAR Genomics and Bioinformatics, Volume 2 (2020) no. 2 | DOI

[8] Cunha, T. J.; de Medeiros, B. A.; Lord, A.; Sørensen, M. V.; Giribet, G. Rampant loss of universal metazoan genes revealed by a chromosome-level genome assembly of the parasitic Nematomorpha, Current Biology, Volume 33 (2023) no. 16 | DOI

[9] De Coster, W.; D’Hert, S.; Schultz, D. T.; Cruts, M.; Van Broeckhoven, C. NanoPack: visualizing and processing long-read sequencing data, Bioinformatics, Volume 34 (2018) no. 15, pp. 2666-2669 | DOI

[10] De Villalobos, L. C.; Ribera, I.; Downie, I. S. Hairworms found in Scottish agricultural land, with descriptions of two new species of Gordionus Muller (Nematomorpha: Gordiidae), Journal of Natural History, Volume 33 (1999) no. 12, pp. 1767-1780 | DOI

[11] Dobin, A.; Davis, C. A.; Schlesinger, F.; Drenkow, J.; Zaleski, C.; Jha, S.; Batut, P.; Chaisson, M.; Gingeras, T. R. STAR: ultrafast universal RNA-seq aligner, Bioinformatics, Volume 29 (2012) no. 1, pp. 15-21 | DOI

[12] Eleftheriadi, K. MetazoaPhylogenomicsLab/ChromosomeLevelGenomes: Chromosome-level genome of Gordionus montsenyensis added to the repository (refgenomes), Zenodo, 2024 | DOI

[13] Fernández, R.; Tonzo, V.; Simón Guerrero, C.; Lozano-Fernandez, J.; Martínez-Redondo, G. I.; Balart-García, P.; Aristide, L.; Eleftheriadi, K.; Vargas-Chávez, C. MATEdb, a data repository of high-quality metazoan transcriptome assemblies to accelerate phylogenomic studies, Peer Community Journal, Volume 2 (2022) | DOI

[14] Flynn, J. M.; Hubley, R.; Goubert, C.; Rosen, J.; Clark, A. G.; Feschotte, C.; Smit, A. F. RepeatModeler2 for automated genomic discovery of transposable element families, Proceedings of the National Academy of Sciences, Volume 117 (2020) no. 17, pp. 9451-9457 | DOI

[15] Folmer, O.; Black, M. J.; Hoeh, W. R.; Lutz, R. A.; Vrijenhoek, R. C. DNA Primers for Amplification of Mitochondrial Cytochrome c Oxidase Subunit I from Diverse Metazoan Invertebrates, Mol Mar Biol Biotechnol., Volume 3 (1994) no. 5, pp. 294-299

[16] Gabriel, L.; Hoff, K. J.; Brůna, T.; Borodovsky, M.; Stanke, M. TSEBRA: transcript selector for BRAKER, BMC Bioinformatics, Volume 22 (2021) no. 1 | DOI

[17] Gerlach, S. Nematomorpha In: Limnofauna Europaea. Illies, J. (ed.)., Gustav Fischer Verlag, Stuttgart (1978), pp. 50-53

[18] Guan, D.; McCarthy, S. A.; Wood, J.; Howe, K.; Wang, Y.; Durbin, R. Identifying and removing haplotypic duplication in primary genome assemblies, Bioinformatics, Volume 36 (2020) no. 9, pp. 2896-2898 | DOI

[19] Guiglielmoni, N.; Houtain, A.; Derzelle, A.; Van Doninck, K.; Flot, J.-F. Overcoming uncollapsed haplotypes in long-read assemblies of non-model organisms, BMC Bioinformatics, Volume 22 (2021) no. 1 | DOI

[20] Hanelt, B.; Thomas, F.; Schmidt-Rhaesa, A. Biology of the Phylum Nematomorpha, Advances in Parasitology Volume 59, Elsevier, 2005, pp. 243-305 | DOI

[21] Hanelt, B.; Jr. Janovy, J. Spanning the gap: experimental determination of paratenic host specificity of horsehair worms (Nematomorpha: Gordiida), Invertebrate Biology, Volume 122 (2003) no. 1, pp. 12-18 | DOI

[22] Hoff, K. J.; Lange, S.; Lomsadze, A.; Borodovsky, M.; Stanke, M. BRAKER1: Unsupervised RNA-Seq-Based Genome Annotation with GeneMark-ET and AUGUSTUS, Bioinformatics, Volume 32 (2015) no. 5, pp. 767-769 | DOI

[23] Holley, G.; Beyter, D.; Ingimundardottir, H.; Møller, P. L.; Kristmundsdottir, S.; Eggertsson, H. P.; Halldorsson, B. V. Ratatosk: hybrid error correction of long reads enables accurate variant calling and assembly, Genome Biology, Volume 22 (2021) no. 1 | DOI

[24] Howe, K.; Chow, W.; Collins, J.; Pelan, S.; Pointon, D.-L.; Sims, Y.; Torrance, J.; Tracey, A.; Wood, J. Significantly improving the quality of genome assemblies through curation, GigaScience, Volume 10 (2021) no. 1 | DOI

[25] Kalyaanamoorthy, S.; Minh, B. Q.; Wong, T. K. F.; von Haeseler, A.; Jermiin, L. S. ModelFinder: fast model selection for accurate phylogenetic estimates, Nature Methods, Volume 14 (2017) no. 6, pp. 587-589 | DOI

[26] Katoh, K.; Standley, D. M. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability, Molecular Biology and Evolution, Volume 30 (2013) no. 4, pp. 772-780 | DOI

[27] Kolmogorov, M.; Yuan, J.; Lin, Y.; Pevzner, P. A. Assembly of long, error-prone reads using repeat graphs, Nature Biotechnology, Volume 37 (2019) no. 5, pp. 540-546 | DOI

[28] Langmead, B.; Wilks, C.; Antonescu, V.; Charles, R. Scaling read aligners to hundreds of threads on general-purpose processors, Bioinformatics, Volume 35 (2018) no. 3, pp. 421-432 | DOI

[29] Laumer, C. E.; Fernández, R.; Lemer, S.; Combosch, D.; Kocot, K. M.; Riesgo, A.; Andrade, S. C. S.; Sterrer, W.; Sørensen, M. V.; Giribet, G. Revisiting metazoan phylogeny with genomic sampling of all phyla, Proceedings of the Royal Society B: Biological Sciences, Volume 286 (2019) no. 1906 | DOI

[30] Li, H. Minimap2: pairwise alignment for nucleotide sequences, Bioinformatics, Volume 34 (2018) no. 18, pp. 3094-3100 | DOI

[31] Lomsadze, A.; Burns, P. D.; Borodovsky, M. Integration of mapped RNA-Seq reads into automatic training of eukaryotic gene finding algorithm, Nucleic Acids Research, Volume 42 (2014) no. 15 | DOI

[32] Manni, M.; Berkeley, M. R.; Seppey, M.; Zdobnov, E. M. BUSCO: Assessing Genomic Data Quality and Beyond, Current Protocols, Volume 1 (2021) no. 12 | DOI

[33] Mapleson, D.; Garcia Accinelli, G.; Kettleborough, G.; Wright, J.; Clavijo, B. J. KAT: a K-mer analysis toolkit to quality control NGS datasets and genome assemblies, Bioinformatics, Volume 33 (2016) no. 4, pp. 574-576 | DOI

[34] Marijon, P.; Chikhi, R.; Varré, J.-S. yacrd and fpa: upstream tools for long-read genome assembly, Bioinformatics, Volume 36 (2020) no. 12, pp. 3894-3896 | DOI

[35] Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads, EMBnet.journal, Volume 17 (2011) no. 1 | DOI

[36] Marçais, G.; Kingsford, C. A fast, lock-free approach for efficient parallel counting of occurrences of k-mers, Bioinformatics, Volume 27 (2011) no. 6, pp. 764-770 | DOI

[37] Matthey-Doret, C.; Baudry, L.; Bignaud, A.; Montagne, R.; Guiglielmoni, N.; Foutel-Rodier, T.; Scolari, V. F. hicstuff: Simple library/pipeline to generate and handle Hi-C data, Zenodo (2020) | DOI

[38] Meng, G.; Li, Y.; Yang, C.; Liu, S. MitoZ: a toolkit for animal mitochondrial genome assembly, annotation and visualization, Nucleic Acids Research, Volume 47 (2019) no. 11 | DOI

[39] Minh, B. Q.; Schmidt, H. A.; Chernomor, O.; Schrempf, D.; Woodhams, M. D.; von Haeseler, A.; Lanfear, R. IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era, Molecular Biology and Evolution, Volume 37 (2020) no. 5, pp. 1530-1534 | DOI

[40] Nachtigall, P. G.; Grazziotin, F. G.; Junqueira-de-Azevedo, I. L. M. MITGARD: an automated pipeline for mitochondrial genome assembly in eukaryotic species using RNA-seq data, Briefings in Bioinformatics, Volume 22 (2021) no. 5 | DOI

[41] Opazo, J. Embarking on a novel journey in metazoa evolution through the pioneering sequencing of a key underrepresented lineage, Peer Community in Genomics (2024) | DOI

[42] Ranallo-Benavidez, T. R.; Jaron, K. S.; Schatz, M. C. GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes, Nature Communications, Volume 11 (2020) no. 1 | DOI

[43] Schmidt-Rhaesa, A.; Cieslak, A. Three new species of Paragordionus and Gordionus (Nematomorpha, Gordiida) from Spain and Turkey, with comments on the taxon Semigordionus, Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut, Volume 105 (2008), pp. 13-22

[44] Schmidt-Rhaesa, A. Nematomorpha, Priapulida, Kinorhyncha, Loricifera, 1 11, De Gruyter, 2013 | DOI

[45] Schmidt-Rhaesa, A.; Farfan, M. A.; Bernard, E. C. First Record of Millipeds as Hosts for Horsehair Worms (Nematomorpha) in North America, Northeastern Naturalist, Volume 16 (2009) no. 1, pp. 125-130 | DOI

[46] Schmidt-Rhaesa, A.; Gusich, V. V. A new Gordionus MÜLLER, 1927 from Switzerland (Nematomorpha, Gordiida), Revue suisse de zoologie, Volume 117 (2010), pp. 77-82 | DOI

[47] Schmidt-Rhaesa, A.; Hanelt, B.; Reeves, W. K. Redescription and compilation of Nearctic freshwater Nematomorpha (Gordiida), with the description of two new species, Proceedings of the Academy of Natural Sciences of Philadelphia, Volume 153 (2003) no. 1, pp. 77-117 | DOI

[48] Schmidt-Rhaesa, A.; Martínez, J. Gordius gonzalezi, a new species of horsehair worms (Nematomorpha) from Spain, Zootaxa, Volume 4103 (2016) no. 1 | DOI

[49] Smith, D. G. Observations on the morphology and taxonomy of two Parachordodes species (Nematomorpha, Gordioida, Chordodidae) in southern New England (USA), Journal of Zoology, Volume 225 (1991) no. 3, pp. 469-480 | DOI

[50] Srensen, M. V.; Hebsgaard, M. B.; Heiner, I.; Glenner, H.; Willerslev, E.; Kristensen, R. M. New data from an enigmatic phylum: evidence from molecular sequence data supports a sister-group relationship between Loricifera and Nematomorpha, Journal of Zoological Systematics and Evolutionary Research, Volume 46 (2008) no. 3, pp. 231-239 | DOI

[51] Stanke, M.; Diekhans, M.; Baertsch, R.; Haussler, D. Using native and syntenically mapped cDNA alignments to improve de novo gene finding, Bioinformatics, Volume 24 (2008) no. 5, pp. 637-644 | DOI

[52] Tarailo‐Graovac, M.; Chen, N. Using RepeatMasker to Identify Repetitive Elements in Genomic Sequences, Current Protocols in Bioinformatics, Volume 25 (2009) no. 1 | DOI

[53] Thomas, F.; Schmidt-Rhaesa, A.; Martin, G.; Manu, C.; Durand, P.; Renaud, F. Do hairworms (Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts?, Journal of Evolutionary Biology, Volume 15 (2002) no. 3, pp. 356-361 | DOI

[54] Xu, M.; Guo, L.; Gu, S.; Wang, O.; Zhang, R.; Peters, B. A.; Fan, G.; Liu, X.; Xu, X.; Deng, L.; Zhang, Y. TGS-GapCloser: A fast and accurate gap closer for large genomes with low coverage of error-prone long reads, GigaScience, Volume 9 (2020) no. 9 | DOI

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