Diversity and evolution of myxozoan minicollagens and nematogalectins

BMC Evolutionary Biology

Dorothée Huchon²  Paulyn Cartwright⁴  Nimrod Rubinstein¹  Arik Diamant³  E Sally Chang⁴  Erez Shpirer² 

[1]Department of Molecular and Cellular Biology, Harvard University, Cambridge, USA

[2]Department of Zoology, Tel Aviv University, Tel Aviv, Israel

[3]National Center for Mariculture, Israel Oceanographic and Limnological Research, Eilat, Israel

[4]Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, USA

关键词: Molecular evolution;    Polypodium;    Myxozoa;    Cnidaria;    Phylum-restricted gene;    Nematocysts;    Polar capsules;   

Others  :  1117931
DOI  :  10.1186/s12862-014-0205-0

 received in 2014-07-01, accepted in 2014-09-19,  发布年份 2014

【 摘 要 】

Background

Myxozoa are a diverse group of metazoan parasites with a very simple organization, which has for decades eluded their evolutionary origin. Their most prominent and characteristic feature is the polar capsule: a complex intracellular structure of the myxozoan spore, which plays a role in host infection. Striking morphological similarities have been found between myxozoan polar capsules and nematocysts, the stinging structures of cnidarians (corals, sea anemones and jellyfish) leading to the suggestion that Myxozoa and Cnidaria share a more recent common ancestry. This hypothesis has recently been supported by phylogenomic evidence and by the identification of a nematocyst specific minicollagen gene in the myxozoan Tetracapsuloides bryosalmonae. Here we searched genomes and transcriptomes of several myxozoan taxa for the presence of additional cnidarian specific genes and characterized these genes within a phylogenetic context.

Results

Illumina assemblies of transcriptome or genome data of three myxozoan species (Enteromyxum leei, Kudoa iwatai, and Sphaeromyxa zaharoni) and of the enigmatic cnidarian parasite Polypodium hydriforme (Polypodiozoa) were mined using tBlastn searches with nematocyst-specific proteins as queries. Several orthologs of nematogalectins and minicollagens were identified. Our phylogenetic analyses indicate that myxozoans possess three distinct minicollagens. We found that the cnidarian repertoire of nematogalectins is more complex than previously thought and we identified additional members of the nematogalectin family. Cnidarians were found to possess four nematogalectin/ nematogalectin-related genes, while in myxozoans only three genes could be identified.

Conclusions

Our results demonstrate that myxozoans possess a diverse array of genes that are taxonomically restricted to Cnidaria. Characterization of these genes provide compelling evidence that polar capsules and nematocysts are homologous structures and that myxozoans are highly degenerate cnidarians. The diversity of minicollagens was higher than previously thought, with the presence of three minicollagen genes in myxozoans. Our phylogenetic results suggest that the different myxozoan sequences are the results of ancient divergences within Cnidaria and not of recent specializations of the polar capsule. For both minicollagen and nematogalectin, our results show that myxozoans possess less gene copies than their cnidarian counter parts, suggesting that the polar capsule gene repertoire was simplified with their reduced body plan.

【 授权许可】

   
2014 Shpirer et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 7.

【 参考文献 】

• [1]Lom J, Dyková I: Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol 2006, 53(1):1-36.
• [2]Kent ML, Andree KB, Bartholomew JL, El-Matbouli M, Desser SS, Devlin RH, Feist SW, Hedrick RP, Hoffmann RW, Khattra J, Hallett SL, Lester RJG, Longshaw M, Palenzeula O, Siddall ME, Xiao CX: Recent advances in our knowledge of the Myxozoa. J Eukaryot Microbiol 2001, 48(4):395-413.
• [3]Yokoyama H, Grabner D, Shirakashi S: Transmission biology of the Myxozoa. [http:/ / www.intechopen.com/ books/ health-and-environment-in-aquacultu re/ transmission-biology-of-the-myxozoa] webciteIn Health and Environment in Aquaculture Edited by Carvalho ED, David GS, Silva RJ. 2012. InTech; 2012: http://www.intechopen.com/books/health-and-environment-in-aquaculture/transmission-biology-of-the-myxozoa
• [4]Funk VA, Olafson RW, Raap M, Smith D, Aitken L, Haddow JD, Wang D, Dawson-Coates JA, Burke RD, Miller KM: Identification, characterization and deduced amino acid sequence of the dominant protease from Kudoa paniformis and K. thyrsites: a unique cytoplasmic cysteine protease. Comp Biochem Physiol B Biochem Mol Biol 2008, 149(3):477-489.
• [5]O’Donoghue P: Protistan parasites and Myxozoa. In Marine parasitology: protistan biodiversity. Edited by Rohde K. CSIRO Publishing, Melbourne; 2005:11-17.
• [6]Lom J, Dyková I: Fine structure of triactinomyxon early stages and sporogony: myxosporean and actinosporean features compared. J Protozool 1992, 39(1):16-27.
• [7]Siddall ME, Martin DS, Bridge D, Desser SS, Cone DK: The demise of a phylum of protists: phylogeny of Myxozoa and other parasitic Cnidaria. J Parasitol 1995, 81(6):961-967.
• [8]Jiménez-Guri E, Philippe H, Okamura B, Holland PWH: Buddenbrockia is a cnidarian worm. Science 2007, 317(5834):116-118.
• [9]Štolc A: Actinomyxidies, nouveau groupe de Mésozoaires parent des Myxosporidies. Bull Int Acad Sci Bohème 1899, 22:1-12.
• [10]Weill R: L’interpretation des Cnidosporidies et la valeur taxonomique de leur cnidome. Leur cycle comparé à la phase larvaire des Narcoméduses cuninides. Travaux Stn Zool Wimereaux 1938, 13:727-744.
• [11]Evans NM, Holder MT, Barbeitos MS, Okamura B, Cartwright P: The phylogenetic position of Myxozoa: exploring conflicting signals in phylogenomic and ribosomal data sets. Mol Biol Evol 2010, 27(12):2733-2746.
• [12]Zrzavý J, Hypša V: Myxozoa, Polypodium, and the origin of the Bilateria: the phylogenetic position of “Endocnidozoa” in light of the rediscovery of Buddenbrockia. Cladistics 2003, 19(2):164-169.
• [13]Evans NM, Lindner A, Raikova EV, Collins AG, Cartwright P: Phylogenetic placement of the enigmatic parasite, Polypodium hydriforme, within the Phylum Cnidaria. BMC Evol Biol 2008, 8:139. BioMed Central Full Text
• [14]Lom J, de Puytorac P: Studies on the myxosporidian ultrastructure and polar capsule development. Protistologica 1965, 1(1):53-65.
• [15]Reft AJ, Daly M: Morphology, distribution, and evolution of apical structure of nematocysts in Hexacorallia. J Morphol 2012, 273(2):121-136.
• [16]Holland JW, Okamura B, Hartikainen H, Secombes CJ: A novel minicollagen gene links cnidarians and myxozoans. Proc R Soc Lond B 2011, 278(1705):546-553.
• [17]Galliot B: Hydra, a fruitful model system for 270 years. Int J Dev Biol 2012, 56(6–8):411-423.
• [18]Milde S, Hemmrich G, Anton-Erxleben F, Khalturin K, Wittlieb J, Bosch TCG: Characterization of taxonomically restricted genes in a phylum-restricted cell type. Genome Biol 2009, 10(1):R8. BioMed Central Full Text
• [19]Balasubramanian PG, Beckmann A, Warnken U, Schnölzer M, Schüler A, Bornberg-Bauer E, Holstein TW, Özbek S: Proteome of Hydra Nematocyst. J Biol Chem 2012, 287(13):9672-9681.
• [20]Kurz EM, Holstein TW, Petri BM, Engel J, David CN: Mini-collagens in Hydra nematocytes. JCell Biol 1991, 115(4):1159-1169.
• [21]David CN, Özbek 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.
• [22]Adamczyk P, Meier S, Gross T, Hobmayer B, Grzesiek S, Bächinger HP, Holstein TW, Özbek S: Minicollagen-15, a novel minicollagen isolated from Hydra, forms tubule structures in nematocysts. J Mol Biol 2008, 376(4):1008-1020.
• [23]Engel U, Oezbek S, Engel R, Petri B, Lottspeich F, Holstein TW: Nowa, a novel protein with minicollagen Cys-rich domains, is involved in nematocyst formation in Hydra. J Cell Sci 2002, 115(20):3923-3934.
• [24]Özbek S, Pokidysheva E, Schwager M, Schulthess T, Tariq N, Barth D, Milbradt AG, Moroder L, Engel J, Holstein TW: 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.
• [25]Koch AW, Holstein TW, Mala C, Kurz E, Engel J, David CN: Spinalin, a new glycine- and histidine-rich protein in spines of Hydra nematocysts. J Cell Sci 1998, 111:1545-1554.
• [26]Hellstern S, Stetefeld J, Fauser C, Lustig A, Engel J, Holstein TW, Özbek S: Structure/function analysis of spinalin, a spine protein of Hydra nematocysts. FEBS J 2006, 273(14):3230-3237.
• [27]Hwang JS, Takaku Y, Momose T, Adamczyk P, Özbek S, Ikeo K, Khalturin K, Hemmrich G, Bosch TCG, Holstein TW, David CN, Gojobori T: 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.
• [28]Adamczyk P, Zenkert C, Balasubramanian PG, Yamada S, Murakoshi S, Sugahara K, Hwang JS, Gojobori T, Holstein TW, Ozbek S: A non-sulfated chondroitin stabilizes membrane tubulation in cnidarian organelles. J Biol Chem 2010, 285(33):25613-25623.
• [29]Ibragimov A, Raikova E: Nematocysts of Polypodium hydriforme, a cnidarian parasite of acipenseriform fishes. Hydrobiologia 2004, 530–531(1–3):165-171.
• [30]Chapman GB, Tilney LG: Cytological studies of the nematocysts of Hydra. II. The stenoteles. J Biophys Biochem Cytol 1959, 5(1):79-84.
• [31]Chapman GB, Tilney LG: Cytological studies of the nematocysts of Hydra. I. Desmonemes, isorhizas, cnidocils and supporting structures. J Biophys Biochem Cytol 1959, 5(1):69-77.
• [32]Zenkert C, Takahashi T, Diesner MO, Ozbek S: Morphological and molecular analysis of the Nematostella vectensis cnidom. PLoS One 2011, 6(7):e22725.
• [33]Canning EU, Okamura B: Biodiversity and evolution of the Myxozoa. Adv Parasitol 2003, 56:43-131.
• [34]Tops S, Curry A, Okamura B: Diversity and systematics of the Malacosporea (Myxozoa). Invertebr Biol 2005, 124(4):285-295.
• [35]Stanke M, Tzvetkova A, Morgenstern B: AUGUSTUS at EGASP: using EST, protein and genomic alignments for improved gene prediction in the human genome. Genome Biol 2006, 7(Suppl 1):S11.11-S11.18. BioMed Central Full Text
• [36]Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A: Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011, 29(7):644-652.
• [37]Philippe H, Laurent J: How good are deep phylogenetic trees. Curr Opin Genet Dev 1998, 8(8):616-623.
• [38]Slautterback DB, Fawcett DW: The development of the cnidoblasts of Hydra: an electron microscope study of cell differentiation. J Biophys Biochem Cytol 1959, 5(3):441-452.
• [39]Lom J: Notes on the ultrastructure and sporoblast development in fish parasitizing myxosporidian of the genus Sphaeromyxa. Z Zellforsch Mikrosk Anat 1969, 97(3):416-437.
• [40]Milbradt AG, 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.
• [41]Meier S, Jensen PR, David CN, Chapman J, Holstein TW, Grzesiek S, Özbek S: Continuous molecular evolution of protein-domain structures by single amino acid changes. Curr Biol 2007, 17(2):173-178.
• [42]Cannon Q, Wagner E: Comparison of discharge mechanisms of Cnidarian cnidae and Myxozoan polar capsules. Rev Fish Sci 2003, 11(3):185-219.
• [43]Liao D: Concerted evolution: molecular mechanism and biological implications. Am J Hum Genet 1999, 64(1):24-30.
• [44]Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, Salamov A, Terry A, Shapiro H, Lindquist E, Kapitonov VV, Jurka J, Genikhovich G, Grigoriev IV, Lucas SM, Steele RE, Finnerty JR, Technau U, Martindale MQ, Rokhsar DS: Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 2007, 317(5834):86-94.
• [45]Langmead B, Salzberg SL: Fast gapped-read alignment with Bowtie 2. Nat Methods 2012, 9(4):357-359.
• [46]Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJM, Birol I: ABySS: a parallel assembler for short read sequence data. Genome Res 2009, 19(6):1117-1123.
• [47]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 novotranscript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protocols 2013, 8(8):1494-1512.
• [48]Dunlap WC, Starcevic A, Baranasic D, Diminic J, Zucko J, Gacesa R, van Oppen MJH, Hranueli D, Cullum J, Long PF: KEGG orthology-based annotation of the predicted proteome of Acropora digitifera: ZoophyteBase - an open access and searchable database of a coral genome. BMC Genomics 2013, 14(1):509. BioMed Central Full Text
• [49]Katoh K, Kuma K, Toh H, Miyata T: MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 2005, 33(2):511-518.
• [50]Petersen TN, Brunak S, von Heijne G, Nielsen H: SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 2011, 8(10):785-786.
• [51]Pokidysheva E, Milbradt AG, Meier S, Renner C, Häussinger D, Bächinger HP, Moroder L, Grzesiek S, Holstein TW, Özbek S, Engel J: 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.
• [52]Penn O, Privman E, Ashkenazy H, Landan G, Graur D, Pupko T: GUIDANCE: a web server for assessing alignment confidence scores. Nucleic Acids Res 2010, 38(Web Server issue):W23-W28.
• [53]Abascal F, Zardoya R, Posada D: ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005, 21(9):2104-2105.
• [54]Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O: New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010, 59(3):307-321.
• [55]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(3):539-542.