The myxozoan minicollagen gene repertoire was not simplified by the parasitic lifestyle: computational identification of a novel myxozoan minicollagen gene
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
19-28399X
Grantová Agentura České Republiky
PubMed
33743585
PubMed Central
PMC7981951
DOI
10.1186/s12864-021-07515-3
PII: 10.1186/s12864-021-07515-3
Knihovny.cz E-zdroje
- Klíčová slova
- Cnidaria, Custom made script, Myxozoa, Phylogeny, Taxonomically restricted genes, Transcriptome,
- MeSH
- fylogeneze MeSH
- genom MeSH
- Myxozoa * genetika MeSH
- paraziti * MeSH
- životní styl MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
BACKGROUND: Lineage-specific gene expansions represent one of the driving forces in the evolutionary dynamics of unique phylum traits. Myxozoa, a cnidarian subphylum of obligate parasites, are evolutionarily altered and highly reduced organisms with a simple body plan including cnidarian-specific organelles and polar capsules (a type of nematocyst). Minicollagens, a group of structural proteins, are prominent constituents of nematocysts linking Myxozoa and Cnidaria. Despite recent advances in the identification of minicollagens in Myxozoa, the evolutionary history and diversity of minicollagens in Myxozoa and Cnidaria remain elusive. RESULTS: We generated new transcriptomes of two myxozoan species using a novel pipeline for filtering of closely related contaminant species in RNA-seq data. Mining of our transcriptomes and published omics data confirmed the existence of myxozoan Ncol-4, reported only once previously, and revealed a novel noncanonical minicollagen, Ncol-5, which is exclusive to Myxozoa. Phylogenetic analyses support a close relationship between myxozoan Ncol-1-3 with minicollagens of Polypodium hydriforme, but suggest independent evolution in the case of the myxozoan minicollagens Ncol-4 and Ncol-5. Additional genome- and transcriptome-wide searches of cnidarian minicollagens expanded the dataset to better clarify the evolutionary trajectories of minicollagen. CONCLUSIONS: The development of a new approach for the handling of next-generation data contaminated by closely related species represents a useful tool for future applications beyond the field of myxozoan research. This data processing pipeline allowed us to expand the dataset and study the evolution and diversity of minicollagen genes in Myxozoa and Cnidaria. We identified a novel type of minicollagen in Myxozoa (Ncol-5). We suggest that the large number of minicollagen paralogs in some cnidarians is a result of several recent large gene multiplication events. We revealed close juxtaposition of minicollagens Ncol-1 and Ncol-4 in myxozoan genomes, suggesting their common evolutionary history. The unique gene structure of myxozoan Ncol-5 suggests a specific function in the myxozoan polar capsule or tubule. Despite the fact that myxozoans possess only one type of nematocyst, their gene repertoire is similar to those of other cnidarians.
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Okamura B, Gruhl A, Bartholomew JL. An Introduction to Myxozoan Evolution, Ecology and Development. In: Okamura B, Gruhl A, Bartholomew JL, editors. Myxozoan Evolution, Ecology and Development: Switzerland: Springer International Publishing; 2015:1–20. 10.1007/978-3-319-14753-6.
El-Matbouli M, Hoffmann RW, Mandok C. Light and electron-microscopic observations on the route of the triactinomyxon-sporoplasm of Myxobolus cerebralis from epidermis into rainbow trout cartilage. J Fish Biol. 1995;46:919–935.
Gurley RR. The Myxosporidia, or psorosperms of fishes. Report of the commisioner of fish and fisheries 1894;267–302.
Weill R. L'interpretation des cnidosporidies et la valeur taxonomique de leur cnidome. Leur cycle compare a la phase larvaire des narcomeduses cuninides. Trav Stn Zool Wimereux. 1938;13:724–744.
Lom J, Puytorac P. Studies on the myxosporidian ultrastructure and polar capsule development. Protistologica. 1965;1:53–65.
Lom J. Notes on ultrastructure and sporoblast development in fish parasitizing myxosporidian of genus Sphaeromyxa. Z Zellforsch Mikrosk Anat. 1969;97(3):416–437. doi: 10.1007/BF00968848. PubMed DOI
Holland J, Okamura B, Hartikainen H, Secombes C. A novel minicollagen gene links cnidarians and myxozoans. P Roy Sox B-Biol Sci. 2011;278:546–553. PubMed PMC
Khalturin K, Anton-Erxleben F, Sassmann S, Wittlieb J, Hemmrich G, Bosch T. A novel gene family controls species-specific morphological traits in Hydra. PLoS Biol. 2008;6:2436–2449. doi: 10.1371/journal.pbio.0060278. PubMed DOI PMC
Milde S, Hemmrich G, Anton-Erxleben F, Khalturin K, Wittlieb J, Bosch T. Characterization of taxonomically restricted genes in a phylum-restricted cell type. Genome Biol. 2009;10(1):R8. doi: 10.1186/gb-2009-10-1-r8. PubMed DOI PMC
Hwang JS, Takaku Y, Momose T, Adamczyk P, Ozbek S, Ikeo K, Khalturin K, Hemmrich G, Bosch TC, Holstein TW, et al. Nematogalectin, a nematocyst protein with GlyXY and galectin domains, demonstrates nematocyte-specific alternative splicing in Hydra. Proc Natl Acad Sci U S A. 2010;107(43):18539–18544. doi: 10.1073/pnas.1003256107. PubMed DOI PMC
Adamczyk P, Meier S, Gross T, Hobmayer B, Grzesiek S, Bächinger HP, Holstein TW, Ozbek S. Minicollagen-15, a novel minicollagen isolated from Hydra, forms tubule structures in nematocysts. J Mol Biol. 2008;376(4):1008–1020. doi: 10.1016/j.jmb.2007.10.090. PubMed DOI
Tursch A, Mercadante D, Tennigkeit J, Gräter F, Ozbek S. Minicollagen cysteine-rich domains encode distinct modes of polymerization to form stable nematocyst capsules. Sci Rep. 2016;6(1):25709. doi: 10.1038/srep25709. PubMed DOI PMC
David CN, Ozbek S, Adamczyk P, Meier S, Pauly B, Chapman J, Hwang JS, Gojobori T, Holstein TW. Evolution of complex structures: minicollagens shape the cnidarian nematocyst. Trends Genet. 2008;24(9):431–438. doi: 10.1016/j.tig.2008.07.001. PubMed DOI
Kurz E, Holstein T, Petri B, Engel J, David C. Minicollagens in Hydra nematocysts. J Cell Biol. 1991;115(4):1159–1169. doi: 10.1083/jcb.115.4.1159. PubMed DOI PMC
Wang W, Omori M, Hayashibara T, Shimoike K, Hatta M, Sugiyama T, Fujisawa T. Isolation and characterization of a mini-collagen gene encoding a nematocyst capsule protein from a reef-building coral, Acropora donei. Gene. 1995;152(2):195–200. doi: 10.1016/0378-1119(95)00644-L. PubMed DOI
Ozbek S, Pertz O, Schwager M, Lustig A, Holstein T, Engel J. Structure/function relationships in the minicollagen of Hydra nematocysts. J Biol Chem. 2002;277(51):49200–49204. doi: 10.1074/jbc.M209401200. PubMed DOI
Hwang JS, Ohyanagi H, Hayakawa S, Osato N, Nishimiya-Fujisawa C, Ikeo K, David C, Fujisawa T, Gojobori T. The evolutionary emergence of cell type-specific genes inferred from the gene expression analysis of Hydra. Proc Natl Acad Sci U S A. 2007;104(37):14735–14740. doi: 10.1073/pnas.0703331104. PubMed DOI PMC
Ozbek S, Pokidysheva E, Schwager M, Schulthess T, Tariq N, Barth D, Milbradt A, Moroder L, Engel J, Holstein T. The glycoprotein NOWA and minicollagens are part of a disulfide-linked polymer that forms the cnidarian nematocyst wall. J Biol Chem. 2004;279(50):52016–52023. doi: 10.1074/jbc.M407613200. PubMed DOI
Shpirer E, Chang ES, Diamant A, Rubinstein N, Cartwright P, Huchon D. Diversity and evolution of myxozoan minicollagens and nematogalectins. BMC Evol Biol. 2014;14(1):205. doi: 10.1186/s12862-014-0205-0. PubMed DOI PMC
Cannon C, Wagner E. Comparison of discharge mechanisms of cnidarian Cnidae and Myxozoan polar capsules. Rev Fish Sci Aquac. 2003;11(3):185–219. doi: 10.1080/10641260390244305. DOI
Okamura B, Gruhl A, Reft AJ. Cnidarian Origins of the Myxozoa. In: Okamura B, Gruhl A, Bartholomew JL, editors. Myxozoan Evolution, Ecology and Development: Switzerland: Springer International Publishing; 2015:45–68. 10.1007/978-3-319-14753-6.
Foox J, Ringuette M, Desser SS, Siddall ME. In silico hybridization enables transcriptomic illumination of the nature and evolution of Myxozoa. BMC Genomics. 2015;16(1):840. doi: 10.1186/s12864-015-2039-6. PubMed DOI PMC
Americus B, Lotan T, Bartholomew JL, Atkinson SD. A comparison of the structure and function of nematocysts in free-living and par-asitic cnidarians (Myxozoa) Int J Parasitol. 2020;50(10-11):763–769. doi: 10.1016/j.ijpara.2020.04.012. PubMed DOI
Balasubramanian P, Beckmann A, Warnken U, Schnolzer M, Schuler A, Bornberg-Bauer E, Holstein T, Ozbek S. Proteome of Hydra nematocyst. J Biol Che. 2012;287(13):9672–9681. doi: 10.1074/jbc.M111.328203. PubMed DOI PMC
Rachamim T, Morgenstern D, Aharonovich D, Brekhman V, Lotan T, Sher D. The dynamically evolving nematocyst content of an Anthozoan, a scyphozoan, and a hydrozoan. Mol Biol Evol. 2015;32(3):740–753. doi: 10.1093/molbev/msu335. PubMed DOI
Siddall M, Martin D, Bridge D, Desser S, Cone D. The demise of a phylum of protists: phylogeny of Myxozoa and other parasitic Cnidaria. J Parasitol. 1995;81(6):961–967. doi: 10.2307/3284049. PubMed DOI
Zrzavý J, Mihulka S, Kepka P, Bezdek A, Tietz D. Phylogeny of the Metazoa based on morphological and 18S ribosomal DNA evidence. Cladistics. 1998;14(3):249–285. doi: 10.1111/j.1096-0031.1998.tb00338.x. PubMed DOI
Jimenez-Guri E, Philippe H, Okamura B, Holland P. Buddenbrockia is a cnidarian worm. Science. 2007;317(5834):116–118. doi: 10.1126/science.1142024. PubMed DOI
Nesnidal MP, Helmkampf M, Bruchhaus I, El-Matbouli M, Hausdorf B. Agent of whirling disease meets orphan worm: phylogenomic analyses firmly place Myxozoa in Cnidaria. PLoS One. 2013;8(1):e54576. doi: 10.1371/journal.pone.0054576. PubMed DOI PMC
Chang ES, Neuhof M, Rubinstein ND, Diamant A, Philippe H, Huchon D, Cartwright P. Genomic insights into the evolutionary origin of Myxozoa within Cnidaria. Proc Natl Acad Sci U S A. 2015;112(48):14912–14917. doi: 10.1073/pnas.1511468112. PubMed DOI PMC
Lom J, Dykova I, Feist S. Myxosporea–induced xenoma formation in pike (Esox lucius L) renal corpuscles associated with Myxidium lieberkuehni infection. Eur J Protistol. 1989;24(3):271–280. doi: 10.1016/S0932-4739(89)80064-1. PubMed DOI
Weißenberg R. Mikrosporidien und Chlamydozoen als Zellparasiten von Fischen. Verh Dtsch Zool. 1922;27:41–43.
Debaisieux P. Hypertrophie des cellules animales parasitees par des Cnidosporidies. C R Soc Biol. 1919;82:867–869.
Debaisieux P. Notes sur le Myxidium lieberkuehni Bütsch. Celulle. 1920;30:281–290.
Sokolov S, Volkova E, Kudryavtsev A, Parshukov A. Nephrocystidium pickii Weissenberg, 1921 belongs to Myxozoa (Cnidaria) but is not conspecific with Myxidium lieberkuehni Bütschli, 1882 (Myxozoa: Bivalvulida: Variisporina: Myxidiidae): molecular-genetic evidence. Syst Parasitol. 2019;96(1):15–22. doi: 10.1007/s11230-018-9834-9. PubMed DOI
Cibulskis K, McKenna A, Fennell T, Banks E, DePristo M, Getz G. ContEst: estimating cross-contamination of human samples in next-generation sequencing data. Bioinformatics. 2011;27(18):2601–2602. doi: 10.1093/bioinformatics/btr446. PubMed DOI PMC
Lafond-Lapalme J, Duceppe MP, Wang S, Moffett P, Mimee B. A new method for decontamination of de novo transcriptomes using a hierarchical clustering algorithm. Bioinformatics. 2017;33(9):1293–1300. doi: 10.1093/bioinformatics/btw793. PubMed DOI
Simion P, Belkhir K, François C, Veyssier J, Rink JC, Manuel M, Philippe H, Telford MJ. A software tool ‘CroCo’ detects pervasive cross-species contamination in next generation sequencing data. BMC Biol. 2018;16:28. doi: 10.1186/s12915-018-0486-7. PubMed DOI PMC
Piriatinskiy G, Atkinson S, Park S, Morgenstern D, Brekhman V, Yossifon G, Bartholomew J, Lotan T. Functional and proteomic analysis of Ceratonova shasta (Cnidaria: Myxozoa) polar capsules reveals adaptations to parasitism. Sci Rep. 2017;7(1):9010. doi: 10.1038/s41598-017-09955-y. PubMed DOI PMC
Khalturin K, Shinzato C, Khalturina M, Hamada M, Fujie M, Koyanagi R, Kanda M, Goto H, Anton-Erxleben F, Toyokawa M, Toshino S, Satoh N. Medusozoan genomes inform the evolution of the jellyfish body plan. Nat Ecol Evol. 2019;3(5):811–822. doi: 10.1038/s41559-019-0853-y. PubMed DOI
Ben-David J, Atkinson SD, Pollak Y, Yossifon G, Shavit U, Bartholomew JL, Lotan T. Myxozoan polar tubules display structural and functional variation. Parasit Vectors. 2016;9(1):549. doi: 10.1186/s13071-016-1819-4. PubMed DOI PMC
Vollrath F. Spiders' webs. Curr Biol. 2005;15(10):R364–R365. doi: 10.1016/j.cub.2005.05.014. PubMed DOI
Barta JR, Martin DS, Liberator PA, Dashkevicz M, Anderson JW, Feighner SD, Elbrecht A, PerkinsBarrow A, Jenkins MC, Danforth HD, et al. Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. J Parasitol. 1997;83(2):262–271. doi: 10.2307/3284453. PubMed DOI
Kent M, Khattra J, Hervio D, Devlin R. Ribosomal DNA sequence analysis of isolates of the PKX myxosporean and their relationship to members of the genus Sphaerospora. J Aquat Anim Health. 1998;10(1):12–21. doi: 10.1577/1548-8667(1998)010<0012:RDSAOI>2.0.CO;2. DOI
Hallett S, Diamant A. Ultrastructure and small-subunit ribosomal DNA sequence of Henneguya lesteri n. sp (Myxosporea), a parasite of sand whiting Sillago analis (Sillaginidae) from the coast of Queensland, Australia. Dis Aquat Org. 2001;46(3):197–212. doi: 10.3354/dao046197. PubMed DOI
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–2120. doi: 10.1093/bioinformatics/btu170. PubMed DOI PMC
Rumble SM, Lacroute P, Dalca AV, Fiume M, Sidow A, Brudno M. SHRiMP: accurate mapping of short color-space reads. PLoS Comput Biol. 2009;5(5):e1000386. doi: 10.1371/journal.pcbi.1000386. PubMed DOI PMC
David M, Dzamba M, Lister D, Ilie L, Brudno M. SHRiMP2: sensitive yet practical SHort read mapping. Bioinformatics. 2011;27(7):1011–1012. doi: 10.1093/bioinformatics/btr046. PubMed DOI
Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, MacManes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, LeDuc RD, Friedman N, Regev A. De novo transcript sequence reconstruction from RNA-seq using the trinity platform for reference generation and analysis. Nat Protoc. 2013;8(8):1494–1512. doi: 10.1038/nprot.2013.084. PubMed DOI PMC
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(12):1647–1649. doi: 10.1093/bioinformatics/bts199. PubMed DOI PMC
Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Geer LY, Bryant SH. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res. 2017;45(D1):D200–D203. doi: 10.1093/nar/gkw1129. PubMed DOI PMC
Petersen T, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods. 2011;8(10):785–786. doi: 10.1038/nmeth.1701. PubMed DOI
Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC
Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30(9):1312–1313. doi: 10.1093/bioinformatics/btu033. PubMed DOI PMC
Abascal F, Zardoya R, Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics. 2005;21(9):2104–2105. doi: 10.1093/bioinformatics/bti263. PubMed DOI
Le SQ, Gascuel O. An improved general amino acid replacement matrix. Mol Biol Evol. 2008;25(7):1307–1320. doi: 10.1093/molbev/msn067. PubMed DOI
Ronquist F, Teslenko M, van der Mark P, Ayres D, Darling A, Hohna S, Larget B, Liu L, Suchard M, Huelsenbeck J. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61(3):539–542. doi: 10.1093/sysbio/sys029. PubMed DOI PMC
Pokidysheva E, Milbradt A, Meier S, Renner C, Haussinger D, Bachinger H, Moroder L, Grzesiek S, Holstein T, Ozbek S, et al. The structure of the Cys-rich terminal domain of Hydra minicollagen, which is involved in disulfide networks of the nematocyst wall. J Biol Chem. 2004;279(29):30395–30401. doi: 10.1074/jbc.M403734200. PubMed DOI
Milbradt A, Boulegue C, Moroder L, Renner C. The two cysteine-rich head domains of minicollagen from Hydra nematocysts differ in their cystine framework and overall fold despite an identical cysteine sequence pattern. J Mol Biol. 2005;354(3):591–600. doi: 10.1016/j.jmb.2005.09.080. PubMed DOI
Kelley L, Mezulis S, Yates C, Wass M, Sternberg M. The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc. 2015;10(6):845–858. doi: 10.1038/nprot.2015.053. PubMed DOI PMC
Yang J, Yan R, Roy A, Xu D, Poisson J, Zhang Y. The I-TASSER suite: protein structure and function prediction. Nat Methods. 2015;12(1):7–8. doi: 10.1038/nmeth.3213. PubMed DOI PMC
Maiti R, Van Domselaar G, Zhang H, Wishart D. SuperPose: a simple server for sophisticated structural superposition. Nucleic Acids Res. 2004;32:W590–W594. doi: 10.1093/nar/gkh477. PubMed DOI PMC
Laskowski RA. PDBsum: summaries and analyses of PDB structures. Nucleic Acids Res. 2001;29(1):221–222. doi: 10.1093/nar/29.1.221. PubMed DOI PMC
Lüthy R, Bowie JU, Eisenberg D. Assessment of protein models with three-dimensional profiles. Nature. 1992;356(6364):83–85. doi: 10.1038/356083a0. PubMed DOI
Yang Y, Xiong J, Zhou Z, Huo F, Miao W, Ran C, Liu Y, Zhang J, Feng J, Wang M, Wang M, Wang L, Yao B. The genome of the myxosporean Thelohanellus kitauei shows adaptations to nutrient acquisition within its fish host. Genome Biol Evol. 2014;6(12):3182–3198. doi: 10.1093/gbe/evu247. PubMed DOI PMC
Stanke M, Keller O, Gunduz I, Hayes A, Waack S, Morgenstern B. AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 2006;34:W435–W439. doi: 10.1093/nar/gkl200. PubMed DOI PMC