Highly resolved genome assembly and comparative transcriptome profiling reveal genes related to developmental stages of tapeworm Ligula intestinalis
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články
PubMed
38290545
PubMed Central
PMC10827431
DOI
10.1098/rspb.2023.2563
Knihovny.cz E-zdroje
- Klíčová slova
- Cestoda, life cycle, parasite, reference genome, transcriptome,
- MeSH
- Cestoda * genetika MeSH
- cestodózy * parazitologie MeSH
- ryby genetika MeSH
- sperma MeSH
- stanovení celkové genové exprese MeSH
- transkriptom MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
Ligula intestinalis (Cestoda: Diphyllobothriidae) is an emerging model organism for studies on parasite population biology and host-parasite interactions. However, a well-resolved genome and catalogue of its gene content has not been previously developed. Here, we present the first genome assembly of L. intestinalis, based on Oxford Nanopore Technologies, Illumina and Omni-C sequencing methodologies. We use transcriptome profiling to compare plerocercoid larvae and adult worms and identify differentially expressed genes (DEGs) associated with these life stages. The genome assembly is 775.3 mega (M)bp in size, with scaffold N50 value of 118 Mbp and encodes 27 256 predicted protein-coding sequences. Over 60% of the genome consists of repetitive sequences. Synteny analyses showed that the 10 largest scaffolds representing 75% of the genome display high correspondence to full chromosomes of cyclophyllidean tapeworms. Mapping RNA-seq data to the new reference genome, we identified 3922 differentially expressed genes in adults compared with plerocercoids. Gene ontology analyses revealed over-represented genes involved in reproductive development of the adult stage (e.g. sperm production) and significantly enriched DEGs associated with immune evasion of plerocercoids in their fish host. This study provides the first insights into the molecular biology of L. intestinalis and provides the most highly contiguous assembly to date of a diphyllobothriid tapeworm useful for population and comparative genomic investigations of parasitic flatworms.
Department of Evolution Ecology and Behavior University of Illinois Urbana Champaign IL 61801 USA
Faculty of Science University of South Bohemia České Budějovice Czech Republic
Institute of Parasitology Biology Centre CAS České Budějovice Czech Republic
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Auld SKJR, Tinsley MC. 2015. The evolutionary ecology of complex lifecycle parasites: linking phenomena with mechanisms. Heredity (Edinb). 114, 125-132. (10.1038/hdy.2014.84) PubMed DOI PMC
Wang S, et al. 2016. Comparative genomics reveals adaptive evolution of Asian tapeworm in switching to a new intermediate host. Nat. Commun. 7, 1-12. (10.1038/ncomms12845) PubMed DOI PMC
Olson PD, et al. 2018. Genome-wide transcriptome profiling and spatial expression analyses identify signals and switches of development in tapeworms. Evodevo 9, 1-29. (10.1186/s13227-018-0110-5) PubMed DOI PMC
Kikuchi T, et al. 2021. Genome of the fatal tapeworm Sparganum proliferum uncovers mechanisms for cryptic life cycle and aberrant larval proliferation. Commun. Biol. 4, 649. (10.1038/s42003-021-02160-8) PubMed DOI PMC
Li W-H, Yang Y, Zhang N-Z, Wang J-K, Liu Y-J, Li L, Yan H-B, Jia W-Z, Fu B. 2021. Comparative transcriptome analyses of the developmental stages of Taenia multiceps. Front. Vet. Sci. 8, 677045. (10.3389/fvets.2021.677045) PubMed DOI PMC
Liu SN, Su XY, Chen WQ, Yu JW, Li JR, Jiang P, Cui J, Wang ZQ, Zhang X. 2022. Transcriptome profiling of plerocercoid and adult developmental stages of the neglected medical tapeworm Spirometra erinaceieuropaei. Acta Trop. 232, 106483. (10.1016/j.actatropica.2022.106483) PubMed DOI
Hébert FO, Grambauer S, Barber I, Landry CR, Aubin-Horth N. 2016. Transcriptome sequences spanning key developmental states as a resource for the study of the cestode Schistocephalus solidus, a threespine stickleback parasite. Gigascience 5, s13742-016. (10.1186/s13742-016-0128-3) PubMed DOI PMC
Tsai IJ, et al. 2013. The genomes of four tapeworm species reveal adaptations to parasitism. Nature 496, 57-63. (10.1038/nature12031) PubMed DOI PMC
Li W, et al. 2018. The genome of tapeworm Taenia multiceps sheds light on understanding parasitic mechanism and control of coenurosis disease. DNA Res. 25, 499-510. (10.1093/dnares/dsy020) PubMed DOI PMC
Olson PD, Tracey A, Baillie A, James K, Doyle SR, Buddenborg SK, Rodgers FH, Holroyd N, Berriman M. 2020. Complete representation of a tapeworm genome reveals chromosomes capped by centromeres, necessitating a dual role in segregation and protection. BMC Biol. 18, 1-16. (10.1186/s12915-020-00899-w) PubMed DOI PMC
Liu G-H, et al. 2021. Dipylidium caninum draft genome - a new resource for comparative genomic and genetic explorations of flatworms. Genomics 113, 1272-1280. (10.1016/j.ygeno.2021.02.019) PubMed DOI
Pu L, et al. 2022. A chromosome-level genome assembly for the rabbit tapeworm Taenia pisiformis. Gene 834, 146650. (10.1016/j.gene.2022.146650) PubMed DOI
Preza M, Calvelo J, Langleib M, Hoffmann F, Castillo E, Koziol U, Iriarte A. 2021. Stage-specific transcriptomic analysis of the model cestode Hymenolepis microstoma. Genomics 113, 620-632. (10.1016/j.ygeno.2021.01.005) PubMed DOI
Korhonen PK, et al. 2022. Chromosome-scale Echinococcus granulosus (genotype G1) genome reveals the Eg95 gene family and conservation of the EG95-vaccine molecule. Commun. Biol. 5, 199. (10.1038/s42003-022-03125-1) PubMed DOI PMC
International Helminth Genomes Consortium. 2017. Comparative genomics of the major parasitic worms International Helminth Genomes Consortium. bioRxiv 51, 236539. (10.1101/236539) DOI
Berger CS, Laroche J, Maaroufi H, Martin H, Moon K-M, Landry CR, Foster LJ, Aubin-Horth N. 2021. The parasite Schistocephalus solidus secretes proteins with putative host manipulation functions. Parasit. Vectors 14, 436. (10.1186/s13071-021-04933-w) PubMed DOI PMC
Caira JN, Jensen K. 2017. Planetary biodiversity inventory (2008–2017): tapeworms from vertebrate bowels of the earth. Natural History Museum, University of Kansas, pp. 463. Lawrence, KS, USA.
Dubinina MN. 1980. Tapeworms (Cestoda, Ligulidae) of the fauna of the USSR. New Delhi, India: Amerind Publishing Company.
Loot G, Francisco P, Santoul F, Lek S, Guégan J-F. 2001. The three hosts of the Ligula intestinalis (Cestoda) life cycle in Lavernose-Lacasse gravel pit, France. Fundam. Appl. Limnol. 152, 511-525. (10.1127/archiv-hydrobiol/152/2001/511) DOI
Nazarizadeh M, et al. 2023. Historical dispersal and host-switching formed the evolutionary history of a globally distributed multi-host parasite – The Ligula intestinalis species complex. Mol. Phylogenet. Evol. 180, 107677. (10.1016/j.ympev.2022.107677) PubMed DOI
Bouzid W, Lek S, Mace M, Ben Hassine O, Etienne R, Legal L, Loot G. 2008. Genetic diversity of Ligula intestinalis (Cestoda: Diphyllobothriidea) based on analysis of inter-simple sequence repeat markers. J. Zool. Syst. Evol. Res. 46, 289-296.
Štefka J, Hypša V, Scholz T. 2009. Interplay of host specificity and biogeography in the population structure of a cosmopolitan endoparasite: microsatellite study of Ligula intestinalis (Cestoda). Mol. Ecol. 18, 1187-1206. (10.1111/j.1365-294X.2008.04074.x) PubMed DOI
Nazarizadeh M, et al. 2022. Different hosts in different lakes: prevalence and population genetic structure of plerocercoids of Ligula intestinalis (Cestoda) in Czech water bodies. Folia Parasitol. (Praha). 69, 18. (10.14411/fp.2022.018) PubMed DOI
Chomzynski P. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction. Anal. Biochem. 162, 156-159. (10.1006/abio.1987.9999) PubMed DOI
Kolmogorov M, Yuan J, Lin Y, Pevzner PA. 2019. Assembly of long, error-prone reads using repeat graphs. Nat. Biotechnol. 37, 540-546. (10.1038/s41587-019-0072-8) PubMed DOI
Warren RL, et al. 2019. ntEdit: scalable genome sequence polishing. Bioinformatics 35, 4430-4432. (10.1093/bioinformatics/btz400) PubMed DOI PMC
Mallet L, Bitard-Feildel T, Cerutti F, Chiapello H. 2017. PhylOligo: a package to identify contaminant or untargeted organism sequences in genome assemblies. Bioinformatics 33, 3283-3285. (10.1093/bioinformatics/btx396) PubMed DOI PMC
Manchanda N, Portwood JL, Woodhouse MR, Seetharam AS, Lawrence-Dill CJ, Andorf CM, Hufford MB. 2020. GenomeQC: a quality assessment tool for genome assemblies and gene structure annotations. BMC Genomics 21, 193. (10.1186/s12864-020-6568-2) PubMed DOI PMC
Gurevich A, Saveliev V, Vyahhi N, Tesler G. 2013. QUAST: quality assessment tool for genome assemblies. Bioinformatics 29, 1072-1075. (10.1093/bioinformatics/btt086) PubMed DOI PMC
Manni M, Berkeley MR, Seppey M, Simão FA, Zdobnov EM. 2021. BUSCO update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. Mol. Biol. Evol. 38, 4647-4654. (10.1093/molbev/msab199) PubMed DOI PMC
Flynn JM, Hubley R, Goubert C, Rosen J, Clark AG, Feschotte C, Smit AF. 2020. RepeatModeler2 for automated genomic discovery of transposable element families. Proc. Natl Acad. Sci. USA 117, 9451-9457. (10.1073/pnas.1921046117) PubMed DOI PMC
Stanke M, Keller O, Gunduz I, Hayes A, Waack S, Morgenstern B. 2006. AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 34, W435-W439. (10.1093/nar/gkl200) PubMed DOI PMC
Korf I. 2004. Gene finding in novel genomes. BMC Bioinf. 5, 1-9. (10.1186/1471-2105-5-59) PubMed DOI PMC
Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. 2013. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15-21. (10.1093/bioinformatics/bts635) PubMed DOI PMC
Chan PP, Lin BY, Mak AJ, Lowe TM. 2021. tRNAscan-SE 2.0: improved detection and functional classification of transfer RNA genes. Nucleic Acids Res. 49, 9077-9096. (10.1093/nar/gkab688) PubMed DOI PMC
Haas B. 2007. TransposonPSI: an application of PSI-blast to mine (retro-) transposon ORF homologies. Cambridge, MA: Broad Institute.
BioBam. 2019. OmicsBox-Bioinformatics made easy. March 3, 2019, https://www.biobam.com/omicsbox.
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J. Mol. Biol. 215, 403-410. (10.1016/S0022-2836(05)80360-2) PubMed DOI
Huerta-Cepas J, et al. 2019. EggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res. 47, D309-D314. (10.1093/nar/gky1085) PubMed DOI PMC
Jones P, et al. 2014. InterProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236-1240. (10.1093/bioinformatics/btu031) PubMed DOI PMC
Bateman A, et al. 2023. UniProt: the Universal Protein Knowledgebase in 2023. Nucleic Acids Res. 51, D523-D531. (10.1093/nar/gkac1052) PubMed DOI PMC
Pruitt KD, Tatusova T, Maglott DR. 2007. NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res. 35, D61-D65. (10.1093/nar/gkl842) PubMed DOI PMC
Finn RD, et al. 2016. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res. 44, D279-D285. (10.1093/nar/gkv1344) PubMed DOI PMC
Hahn C, Bachmann L, Chevreux B. 2013. Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads—a baiting and iterative mapping approach. Nucleic Acids Res. 41, e129. (10.1093/nar/gkt371) PubMed DOI PMC
Carver T, Harris SR, Berriman M, Parkhill J, McQuillan JA. 2012. Artemis: an integrated platform for visualization and analysis of high-throughput sequence-based experimental data. Bioinformatics 28, 464-469. (10.1093/bioinformatics/btr703) PubMed DOI PMC
Emms DM, Kelly S. 2019. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 238. (10.1186/s13059-019-1832-y) PubMed DOI PMC
Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780. (10.1093/molbev/mst010) PubMed DOI PMC
Price MN, Dehal PS, Arkin AP. 2010. FastTree 2 – approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490. (10.1371/journal.pone.0009490) PubMed DOI PMC
Emms DM, Kelly S. 2017. STRIDE: species tree root inference from gene duplication events. Mol. Biol. Evol. 34, 3267-3278. (10.1093/molbev/msx259) PubMed DOI PMC
Sanderson MJ. 2003. r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19, 301-302. PubMed
Mendes FK, Vanderpool D, Fulton B, Hahn MW. 2020. CAFE 5 models variation in evolutionary rates among gene families. Bioinformatics 36, 5516-5518. PubMed
Soderlund C, Nelson W, Shoemaker A, Paterson A. 2006. SyMAP: a system for discovering and viewing syntenic regions of FPC maps. Genome Res. 16, 1159-1168. (10.1101/gr.5396706) PubMed DOI PMC
Soderlund C, Bomhoff M, Nelson WM. 2011. SyMAP v3.4: a turnkey synteny system with application to plant genomes. Nucleic Acids Res. 39, e68. (10.1093/nar/gkr123) PubMed DOI PMC
Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, Salzberg SL. 2004. Versatile and open software for comparing large genomes. Genome Biol. 5, 1-9. (10.1186/gb-2004-5-2-r12) PubMed DOI PMC
Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114-2120. (10.1093/bioinformatics/btu170) PubMed DOI PMC
Danecek P, et al. 2021. Twelve years of SAMtools and BCFtools. Gigascience 10, giab008. (10.1093/gigascience/giab008) PubMed DOI PMC
Liao Y, Smyth GK, Shi W. 2014. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923-930. (10.1093/bioinformatics/btt656) PubMed DOI
Lambert I, Paysant-Le Roux C, Colella S, Martin-Magniette M-L. 2020. DiCoExpress: a tool to process multifactorial RNAseq experiments from quality controls to co-expression analysis through differential analysis based on contrasts inside GLM models. Plant Methods 16, 68. (10.1186/s13007-020-00611-7) PubMed DOI PMC
Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR : a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140. (10.1093/bioinformatics/btp616) PubMed DOI PMC
Wu T, et al. 2021. clusterProfiler 4.0: a universal enrichment tool for interpreting omics data. Innovation 2, 100141. (10.1016/j.xinn.2021.100141) PubMed DOI PMC
Yu G, Wang L-G, Yan G-R, He Q-Y. 2015. DOSE: an R/Bioconductor package for disease ontology semantic and enrichment analysis. Bioinformatics 31, 608-609. (10.1093/bioinformatics/btu684) PubMed DOI
Supek F, Bošnjak M, Škunca N, Šmuc T. 2011. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS ONE 6, e21800. (10.1371/journal.pone.0021800) PubMed DOI PMC
Waeschenbach A, Brabec J, Scholz T, Littlewood DTJ, Kuchta R. 2017. The catholic taste of broad tapeworms – multiple routes to human infection. Int. J. Parasitol. 47, 831-843. (10.1016/j.ijpara.2017.06.004) PubMed DOI
Koonin EV. 2005. Orthologs, paralogs, and evolutionary genomics. Annu. Rev. Genet. 39, 309-338. (10.1146/annurev.genet.39.073003.114725) PubMed DOI
Zhang J. 2003. Evolution by gene duplication: an update. Trends Ecol. Evol. 18, 292-298. (10.1016/S0169-5347(03)00033-8) DOI
Lynch M, Conery JS. 2000. The evolutionary fate and consequences of duplicate genes. Science 290, 1151-1155. (10.1126/science.290.5494.1151) PubMed DOI
Albalat R, Cañestro C. 2016. Evolution by gene loss. Nat. Rev. Genet. 17, 379-391. PubMed
Wang J, Han G-Z. 2023. Genome mining shows that retroviruses are pervasively invading vertebrate genomes. Nat. Commun. 14, 4968. (10.1038/s41467-023-40732-w) PubMed DOI PMC
Mueller JF, Strano AJ. 1974. Sparganum proliferum, a Sparganum infected with a virus? J. Parasitol. 60, 15. (10.2307/3278671) PubMed DOI
Esch GW, Fernández JC. 1993. A functional biology of parasitism. Dordrecht, Netherlands: Springer Netherlands. (10.1007/978-94-011-2352-5) DOI
Finnegan DJ. 2012. Retrotransposons. Curr. Biol. 22, R432-R437. (10.1016/j.cub.2012.04.025) PubMed DOI
Chuong EB, Elde NC, Feschotte C. 2016. Regulatory evolution of innate immunity through co-option of endogenous retroviruses. Science 351, 1083-1087. (10.1126/science.aad5497) PubMed DOI PMC
Conesa A, et al. 2016. A survey of best practices for RNA-seq data analysis. Genome Biol. 17, 13. (10.1186/s13059-016-0881-8) PubMed DOI PMC
Yoneva A, Scholz T, Bruňanská M, Kuchta R. 2015. Vitellogenesis of diphyllobothriidean cestodes (Platyhelminthes). C. R. Biol. 338, 169-179. (10.1016/j.crvi.2015.01.001) PubMed DOI
Varki A, Cummings R, Esko J, Freeze H, Hart G, Marth J. 1999. Glycobiology of Protozoal and Helminthic Parasites. In Essentials of glycobiology. New York, NY: Cold Spring Harbor Laboratory Press. PubMed
Biserova NM, Gordeev II. 2010. Fine structure of nervous system in plerocercoid Ligula intestinalis (Cestoda: Diphyllobothriidea). Invertebr. Zool. 7, 133-154. (10.15298/invertzool.07.2.05) DOI
Justine J-L, Briand MJ, Bray RA. 2012. A quick and simple method, usable in the field, for collecting parasites in suitable condition for both morphological and molecular studies. Parasitol. Res. 111, 341-351. (10.1007/s00436-012-2845-6) PubMed DOI
Ehlers U. 1984. Phylogenetisches system der Plathelminthes. Munich, Germany: Urban & Fischer.
Levron C, Sitko J, Scholz T. 2009. Spermiogenesis and spermatozoon of the yapeworm Ligula intestinalis (Diphyllobothriidea): phylogenetic implications. J. Parasitol. 95, 1-9. (10.1645/GE-1646.1) PubMed DOI
Smyth JD, McManus DP. 1989. The physiology and biochemistry of cestodes. Cambridge, UK: Cambridge University Press. (10.1017/CBO9780511525841) DOI
Yoneva A, Kuchta R, Scholz T. 2014. First study of vitellogenesis of the broad fish tapeworm Diphyllobothrium latum (Cestoda, Diphyllobothriidea), a human parasite with extreme fecundity. Parasitol. Int. 63, 747-753. (10.1016/j.parint.2014.07.002) PubMed DOI
Yoneva A, Scholz T, Młocicki D, Kuchta R. 2015. Ultrastructural study of vitellogenesis of Ligula intestinalis (Diphyllobothriidea) reveals the presence of cytoplasmic-like cell death in cestodes. Front. Zool. 12, 35. (10.1186/s12983-015-0128-7) PubMed DOI PMC
García-Montoya GM, Mesa-Arango JA, Isaza-Agudelo JP, Agudelo-Lopez SP, Cabarcas F, Barrera LF, Alzate JF. 2016. Transcriptome profiling of the cysticercus stage of the laboratory model Taenia crassiceps, strain ORF. Acta Trop. 154, 50-62. (10.1016/j.actatropica.2015.11.001) PubMed DOI
Basika T, et al. 2019. Transcriptomic profile of two developmental stages of the cestode parasite Mesocestoides corti. Mol. Biochem. Parasitol. 229, 35-46. (10.1016/j.molbiopara.2019.02.006) PubMed DOI
Dold C, Holland C V. 2011. Ascaris and ascariasis. Microbes Infect. 13, 632-637. (10.1016/j.micinf.2010.09.012) PubMed DOI
Bouzid W, Štefka J, Hypša V, Lek S, Scholz T, Legal L, Hassine OB, Loot G. 2008. Geography and host specificity: two forces behind the genetic structure of the freshwater fish parasite Ligula intestinalis (Cestoda: Diphyllobothriidae). Int. J. Parasitol. 38, 1465-1479. (10.1016/j.ijpara.2008.03.008) PubMed DOI
Nazarizadeh M, Nováková M, Drábková M, Catchen J, Olson J, Štefka J. 2024. Highly resolved genome assembly and comparative transcriptome profiling reveal genes related to developmental stages of tapeworm ligula intestinalis. Figshare. (10.6084/m9.figshare.c.7021305) PubMed DOI PMC