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Genomic insights into the evolutionary origin of Myxozoa within Cnidaria
Open accessAbstract
The Myxozoa comprise over 2,000 species of microscopic obligate parasites that use both invertebrate and vertebrate hosts as part of their life cycle. Although the evolutionary origin of myxozoans has been elusive, a close relationship with cnidarians, a group that includes corals, sea anemones, jellyfish, and hydroids, is supported by some phylogenetic studies and the observation that the distinctive myxozoan structure, the polar capsule, is remarkably similar to the stinging structures (nematocysts) in cnidarians. To gain insight into the extreme evolutionary transition from a free-living cnidarian to a microscopic endoparasite, we analyzed genomic and transcriptomic assemblies from two distantly related myxozoan species, Kudoa iwatai and Myxobolus cerebralis, and compared these to the transcriptome and genome of the less reduced cnidarian parasite, Polypodium hydriforme. A phylogenomic analysis, using for the first time to our knowledge, a taxonomic sampling that represents the breadth of myxozoan diversity, including four newly generated myxozoan assemblies, confirms that myxozoans are cnidarians and are a sister taxon to P. hydriforme. Estimations of genome size reveal that myxozoans have one of the smallest reported animal genomes. Gene enrichment analyses show depletion of expressed genes in categories related to development, cell differentiation, and cell-cell communication. In addition, a search for candidate genes indicates that myxozoans lack key elements of signaling pathways and transcriptional factors important for multicellular development. Our results suggest that the degeneration of the myxozoan body plan from a free-living cnidarian to a microscopic parasitic cnidarian was accompanied by extreme reduction in genome size and gene content.
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In the citing paper
“Thus, while strong support for Ctenophora-sister may be obtained from phylogenomic datasets (2 -6, 46, 55), our analysis suggests these results are caused by undetected systematic bias.”
From Genomic data do not support comb jellies as the sister group to all other animals (2015) · cites this paper as [55]
Experimental — accuracy not yet measuredIn the citing paper
“The topologies from Chang and Feuda are based on the same data set which is made up of 51,940 amino acid positions from 78 taxa representing a wide range of animals and 9 non-animal outgroups.”
From Six-state amino acid recoding is not an effective strategy to offset the effects of compositional heterogeneity and saturation in phylogenetic analyses (2019) · cites this paper as Chang et al. 2015
In the citing paper
“Porifera-sister generally [6], but not invariably [12, 38], emerges when site-specific differences in amino acid composition are modeled and distant outgroups (e.g., Fungi) are not included in the analyses.”
From Improved Modeling of Compositional Heterogeneity Supports Sponges as Sister to All Other Animals (2017) · cites this paper as [12]
In the citing paper
“We show that two key phylogenomic datasets that previously supported Ctenophora-sister [10, 12] display strong heterogeneity in amino acid composition across sites and taxa”
From Improved Modeling of Compositional Heterogeneity Supports Sponges as Sister to All Other Animals (2017) · cites this paper as [12]
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Genomic data do not support comb jellies as the sister group to all other animals
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BackgroundCtenophore relationships and their placement as the sister group to all other animals
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InfluentialRevisionary systematics of Octocorallia (Cnidaria: Anthozoa) guided by phylogenomics
McFadden, C. S., van Ofwegen, L. P., & Quattrini, A. M. (2022) · Bulletin of the Society of Systematic Biologists · doi:10.18061/bssb.v1i3.8735 · Cited by 182
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BackgroundExtensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts
Steenwyk, J. L., Opulente, D. A., Kominek, J., Shen, X.-X., Zhou, X., Labella, A. L., Bradley, N. P., Eichman, B. F., Čadež, N., Libkind, D., et al. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000255 · Cited by 162
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BackgroundInfluentialEmbracing Uncertainty in Reconstructing Early Animal Evolution
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InfluentialNeural versus alternative integrative systems: molecular insights into origins of neurotransmitters
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BackgroundA cnidarian parasite of salmon (Myxozoa: Henneguya ) lacks a mitochondrial genome
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The Multipartite Mitochondrial Genome of Enteromyxum leei (Myxozoa): Eight Fast-Evolving Megacircles
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“The Medusozoa fall into five distinct classes, Hydrozoa, Scyphozoa, Cubozoa, Staurozoa and the diverse group of obligate parasitic Myxozoa (Chang et al., 2015; Collins et al., 2006; Kayal et al., 2013; Zapata et al., 2015).”
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“We thus report that the addition of morphological characters to phylogenomic data under certain weighting schemes infers Porifera as the SOM, shifting away from the recent preference for Ctenophora as the inferred SOM (Ryan et al. 2013; Chang et al. 2015; Whelan et al. 2015).”
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Amazonian waters harbour an ancient freshwater Ceratomyxa lineage (Cnidaria: Myxosporea)
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“Here we survey what is known in Cnidaria, the clade that forms the sister group to Bilateria and shows a broad array of sexual strategies and sexual plasticity.”
BackgroundResolving tricky nodes in the tree of life through amino acid recoding
Giacomelli, M., Rossi, M. E., Lozano-Fernández, J., Feuda, R., & Pisani, D. (2022) · iScience · doi:10.1016/j.isci.2022.105594 · Cited by 42
“Amino acid datasets analyzed using CAT and CAT-GTR tend to switch between Porifera– (14) and Ctenophora–sister (49) depending on outgroup sampling.”
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A myxozoan genome reveals mosaic evolution in a parasitic cnidarian
Guo, Q., Atkinson, S. D., Xiao, B., Zhai, Y., Bartholomew, J. L., & Gu, Z. (2022) · BMC Biology · doi:10.1186/s12915-022-01249-8 · Cited by 31
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BackgroundResultInfluentialMonophyly of Anthozoa (Cnidaria): why do nuclear and mitochondrial phylogenies disagree?
Pratlong, M., Rancurel, C., Pontarotti, P., & Aurelle, D. (2016) · Zoologica Scripta · doi:10.1111/zsc.12208 · Cited by 37
“…tried to understand the differences between nuclear and mitochondrial phylogenies by analysing our data set and the data sets of Kayal et al. (2013), Chang et al. (2015) and Zapata et al. (2015) in the light of substitution saturation which is a mechanism known to lead to incongruent phylogenies.”
BackgroundMethodResultInfluentialMyxosporea (Myxozoa, Cnidaria) Lack DNA Cytosine Methylation
Kyger, R., Luzuriaga-Neira, A., Layman, T. S., Sandberg, T. O. M., Singh, D., Huchon, D., Peri, S., Atkinson, S. D., Bartholomew, J. L., Yi, S. V., et al. (2020) · Molecular Biology and Evolution · doi:10.1093/molbev/msaa214 · Cited by 31
“hydriforme, an enigmatic parasite of paddlefish and sturgeon oocytes which is the sister taxon to Myxozoa (Chang et al. 2015).”
BackgroundInfluentialSelf-citationTranscriptome Characterization of Reverse Development in Turritopsis dohrnii (Hydrozoa, Cnidaria)
Matsumoto, Y., Piraino, S., & Miglietta, M. P. (2019) · G3 Genes Genomes Genetics · doi:10.1534/g3.119.400487 · Cited by 31
Genomics and the animal tree of life: conflicts and future prospects
Giribet, G. (2016) · Zoologica Scripta · doi:10.1111/zsc.12215 · Cited by 30
“Surprisingly, virtually, all other analyses of metazoan phylogenomics result in ctenophores being more basal than sponges (Ryan et al. 2013; Moroz et al. 2014; Chang et al. 2015; Whelan et al. 2015).”
BackgroundThe complex evolutionary history of sulfoxide synthase in ovothiol biosynthesis
Gerdol, M., Sollitto, M., Pallavicini, A., & Castellano, I. (2019) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2019.1812 · Cited by 30
“For example, the lack of OvoA in organisms that underwent genome reduction along with the simplification of the body plan (e.g. Mesozoa [38]) or in obligated parasites which lost primary metabolic pathways provided by the host (e.g. Platyhelminthes [35,36] and Myxozoa [37]), is perhaps not surprising.”
BackgroundInfluentialFaber, M., Shaw, S., Yoon, S., Alves, E. D. P., Wang, B., Qi, Z., Okamura, B., Hartikainen, H., Secombes, C. J., & Holland, J. W. (2021) · Scientific Reports · doi:10.1038/s41598-020-77881-7 · Cited by 30
Extreme Genome and Nervous System Streamlining in the Invertebrate Parasite Intoshia variabili
Slyusarev, G. S., Starunov, V. V., Bondarenko, A. S., Zorina, N. A., & Bondarenko, N. I. (2020) · Current Biology · doi:10.1016/j.cub.2020.01.061 · Cited by 33
Sasson, D. A., & Ryan, J. F. (2016) · PeerJ · doi:10.7717/peerj.1846 · Cited by 29
Braden, L. M., Rasmussen, K. J., Purcell, S. L., Ellis, L., Mahony, A. A. M., Cho, S., Whyte, S. K., Jones, S. R. M., & Fast, M. D. (2017) · Infection and Immunity · doi:10.1128/iai.00556-17 · Cited by 30
“The Myxozoa are obligate endoparasitic metazoans comprising over 2,000 species (1, 2) and are common parasites of fish, invertebrates, and occasionally vertebrates in”
BackgroundPhylogenomics and the first higher taxonomy of Placozoa, an ancient and enigmatic animal phylum
Tessler, M., Neumann, J. S., Kamm, K., Osigus, H., Eshel, G., Narechania, A., Burns, J. A., DeSalle, R., & Schierwater, B. (2022) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2022.1016357 · Cited by 28
“Placozoans appear to diversify on a fairly long branch in our likelihood trees (Figure 1), implying that while the phylum is ancient, extant members diversified later — potentially several hundred million years after Placozoa diverged from other Metazoa based on our time calibration (Figure 1B).”
BackgroundInfluentialNovosolov, M., Yahalomi, D., Chang, E. S., Fiala, I., Cartwright, P., & Huchon, D. (2022) · Genome Biology and Evolution · doi:10.1093/gbe/evac112 · Cited by 27
Self-citationThe compact genome of the sponge Oopsacas minuta (Hexactinellida) is lacking key metazoan core genes
Santini, S., Schenkelaars, Q., Jourda, C., Duschene, M., Belahbib, H., Rocher, C., Selva, M., Riesgo, A., Vervoort, M., Leys, S. P., et al. (2023) · BMC Biology · doi:10.1186/s12915-023-01619-w · Cited by 28
“So far, the absence of the Wnt pathway was only reported in myxozoans [120], a group of microscopic parasitic cnidarians.”
BackgroundBiodiversity and host-parasite cophylogeny of Sphaerospora (sensu stricto) (Cnidaria: Myxozoa)
Patra, S., Bartošová‐Sojková, P., Pecková, H., Fiala, I., Eszterbauer, E., & Holzer, A. S. (2018) · Parasites & Vectors · doi:10.1186/s13071-018-2863-z · Cited by 27
Cunha, T. J., de Medeiros, B. A. S., Lord, A., Sørensen, M. V., & Giribet, G. (2023) · Current Biology · doi:10.1016/j.cub.2023.07.003 · Cited by 25
Gupta, A., & Kaur, H. (2017) · Microbial Pathogenesis · doi:10.1016/j.micpath.2017.08.044 · Cited by 26
Animal multicellularity and polarity without Wnt signaling
Schenkelaars, Q., Pratlong, M., Kodjabachian, L., Fierro‐Constaín, L., Vacelet, J., Bivic, A. L., Renard, E., & Borchiellini, C. (2017) · Scientific Reports · doi:10.1038/s41598-017-15557-5 · Cited by 26
The onset of regenerative properties in ctenophores
Martindale, M. Q. (2016) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2016.06.017 · Cited by 24
Vernale, A., Prünster, M. M., Marchianò, F., Debost, H., Brouilly, N., Rocher, C., Massey‐Harroche, D., Renard, E., Bivic, A. L., Habermann, B. H., et al. (2021) · BMC Ecology and Evolution · doi:10.1186/s12862-021-01866-x · Cited by 25
Klompen, A. M. L., Kayal, E., Collins, A. G., & Cartwright, P. (2021) · Genome Biology and Evolution · doi:10.1093/gbe/evab081 · Cited by 23
Self-citationHartigan, A., Kosakyan, A., Pecková, H., Eszterbauer, E., & Holzer, A. S. (2020) · BMC Genomics · doi:10.1186/s12864-020-6705-y · Cited by 23
Gene Loss may have Shaped the Cnidarian and Bilaterian Hox and ParaHox Complement
Steinworth, B. M., Martindale, M. Q., & Ryan, J. F. (2022) · Genome Biology and Evolution · doi:10.1093/gbe/evac172 · Cited by 22
Zhang, X., Liu, Y., Whipps, C. M., Guo, Q., & Gu, Z. (2018) · International Journal for Parasitology Parasites and Wildlife · doi:10.1016/j.ijppaw.2018.11.006 · Cited by 22
Moreland, R. T., Nguyen, A., Ryan, J. F., & Baxevanis, A. D. (2020) · Database · doi:10.1093/database/baaa029 · Cited by 20
Alama-Bermejo, G., Meyer, E., Atkinson, S. D., Holzer, A. S., Wiśniewska, M. M., Kolísko, M., & Bartholomew, J. L. (2020) · Genome Biology and Evolution · doi:10.1093/gbe/evaa109 · Cited by 22
A Cnidarian Phylogenomic Tree Fitted With Hundreds of 18S Leaves
DeBiasse, M. B., Buckenmeyer, A., Macrander, J., Babonis, L. S., Bentlage, B., Cartwright, P., Prada, C., Reitzel, A. M., Stampar, S. N., Collins, A. G., et al. (2024) · Bulletin of the Society of Systematic Biologists · doi:10.18061/bssb.v3i2.9267 · Cited by 20
Self-citationda Silva, D. T., Matos, P., Lima, A. M., Furtado, A. P., Hamoy, I. G., & Matos, E. R. (2018) · Parasitology Research · doi:10.1007/s00436-018-6051-z · Cited by 20
Illuminating Genetic Mysteries of the Dead Sea Scrolls
Anava, S., Neuhof, M., Gingold, H., Sagy, O., Munters, A. R., Svensson, E., Afshinnekoo, E., Danko, D., Foox, J., Shor, P., et al. (2020) · Cell · doi:10.1016/j.cell.2020.04.046 · Cited by 21
Self-citationExpansion and collapse of VEGF diversity in major clades of the animal kingdom
Rauniyar, K., Bokharaie, H., & Jeltsch, M. (2023) · Angiogenesis · doi:10.1007/s10456-023-09874-9 · Cited by 19
“kitauei belongs to the endoparasitic myxozoa branch of Cnidaria, which is characterized by a reduction in genome size and gene depletion [58], explaining the lack of PDGF/VEGFs in parasitic Cnidaria.”
BackgroundA deep dive into genome assemblies of non-vertebrate animals
Guiglielmoni, N., Rivera‐Vicéns, R. E., Koszul, R., & Flot, J. (2022) · Peer Community Journal · doi:10.24072/pcjournal.128 · Cited by 16
Ferrández‐Roldán, A., Martí‐Solans, J., Cañestro, C., & Albalat, R. (2019) · Results and problems in cell differentiation · doi:10.1007/978-3-030-23459-1_4 · Cited by 18
Mechanisms and Drivers for the Establishment of Life Cycle Complexity in Myxozoan Parasites
Lisnerová, M., Fiala, I., Cantatore, D. M. P., Irigoitia, M. M., Timi, J. T., Pecková, H., Bartošová‐Sojková, P., Sandoval, C. M., Luer, C. A., Morris, J. J., et al. (2020) · Biology · doi:10.3390/biology9010010 · Cited by 18
“Myxozoans are intriguing group of obligate parasites that evolved at the base of metazoans, showing extremely derived genomes [8] and complex life histories (summarized in [3]).”
BackgroundHow to build single‐celled cnidarians with worm‐like motility: Lessons from Myxozoa
Adriano, E. A., Zatti, S. A., & Okamura, B. (2021) · Journal of Anatomy · doi:10.1111/joa.13566 · Cited by 18
Animal origins and the Tonian Earth system
Mills, D. B., Francis, W. R., & Canfield, D. E. (2018) · Emerging Topics in Life Sciences · doi:10.1042/etls20170160 · Cited by 16
Kosakyan, A., Alama-Bermejo, G., Bartošová‐Sojková, P., Born‐Torrijos, A., Šíma, R., Nenarokova, A., Eszterbauer, E., Bartholomew, J. L., & Holzer, A. S. (2019) · Scientific Reports · doi:10.1038/s41598-019-51479-0 · Cited by 16
Brancaccio, M., Tangherlini, M., Danovaro, R., & Castellano, I. (2021) · Genome Biology and Evolution · doi:10.1093/gbe/evab169 · Cited by 16
Improving Orthologous Signal and Model Fit in Datasets Addressing the Root of the Animal Phylogeny
McCarthy, C. G. P., Mulhair, P. O., Siu-Ting, K., Creevey, C. J., & O’Connell, M. J. (2022) · Molecular Biology and Evolution · doi:10.1093/molbev/msac276 · Cited by 19
“Notably, two datasets previously demonstrated to support Ctenophora-sister instead support Porifera-sister after such reanalysis.”
BackgroundMethodInfluentialGenetic Diversity of Serine Protease Inhibitors in Myxozoan (Cnidaria, Myxozoa) Fish Parasites
Eszterbauer, E., Sipos, D. I. K., Kaján, G. L., Szegő, D., Fiala, I., Holzer, A. S., & Bartošová‐Sojková, P. (2020) · Microorganisms · doi:10.3390/microorganisms8101502 · Cited by 15
“PRJNA261422 and PRJNA261052) [28]; Henneguya salminicola (BioProject No.”
BackgroundXia, W., Li, H., Cheng, W., Li, H., Mi, Y., Gou, X., & Liu, Y. (2020) · Frontiers in Genetics · doi:10.3389/fgene.2020.00535 · Cited by 16
Ahmad, F., Debes, P. V., Pukk, L., Kahar, S., Hartikainen, H., Gross, R., & Vasemägi, A. (2021) · Parasitology · doi:10.1017/s003118202100010x · Cited by 15
“1A, Kraken2 = 6508, BLASTN = 10283 and BLASTX = 6440) reflective of the highly diverged nature of myxozoans from other cnidarians (Chang et al ., 2015) and a small number of available myxozoan genomes.”
InfluentialHartigan, A., Jaimes‐Becerra, A., Okamura, B., Doonan, L. B., Ward, M. A., Marques, A. C., & Long, P. F. (2021) · PeerJ · doi:10.7717/peerj.11208 · Cited by 15
“Phylogenetic tree representing some of the major clades of Cnidaria (based (Chang et al., 2015; Kayal et al., 2018)).”
BackgroundInfluentialAn evolutionary genomics view on neuropeptide genes in Hydrozoa and Endocnidozoa (Myxozoa)
Koch, T. L., Hauser, F., & Grimmelikhuijzen, C. J. P. (2021) · BMC Genomics · doi:10.1186/s12864-021-08091-2 · Cited by 12
“Most of these parasites have complex life cycles, where they alternate between an invertebrate and a vertebrate host, the last one frequently being a fish [60, 68, 76, 77].”
BackgroundInfluentialGupta, A., & Kaur, H. (2018) · Microbial Pathogenesis · doi:10.1016/j.micpath.2018.04.042 · Cited by 15
The Molecular Clock as a Tool for Understanding Host-Parasite Evolution
Warnock, R. C. M., & Engelstädter, J. (2021) · Topics in geobiology · doi:10.1007/978-3-030-52233-9_13 · Cited by 13
Guo, Q., Whipps, C. M., Zhai, Y., Li, D., & Gu, Z. (2022) · Biology · doi:10.3390/biology11010091 · Cited by 14
“They have only recently been classified as cnidarians and, together with Polypodium hydriforme, form a sister clade to Medusozoa [3,35].”
BackgroundInfluential
Metadata
- Authors
- Chang, E. S., Neuhof, M., Rubinstein, N. D., Diamant, A., Philippe, H., Huchon, D., & Cartwright, P.
- Affiliations
- University of Kansas (US)
- Tel Aviv University (IL)
- Harvard University (US)
- Israel Oceanographic and Limnological Research (IL)
- Centre National de la Recherche Scientifique (FR)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2015-11-16
- Volume
- 112
- Issue
- 48
- Pages
- 14912-14917
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC4672818
- OpenAlex
- W2176109601
- Cited by
- 262
- References
- 67
- Citations by year
- 2026: 9 · 2025: 10 · 2024: 18 · 2023: 19 · 2022: 26 · 2021: 47 · 2020: 28 · 2019: 24 · 2018: 29 · 2017: 26 · 2016: 25 · 2015: 1
- FWCI
- 8.92
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- KU ScholarWorks (University of Kansas) (submittedVersion, other-oa)
- Funders
- NSF | BIO | Division of Environmental Biology (0953571)
- NSF | BIO | Division of Integrative Organismal Systems (1321759)
- Israel Science Foundation (663/10)
- United States-Israel Binational Science Foundation (2012768)
- Topics
- Life Sciences › Immunology and Microbiology › Parasitology › Myxozoan Parasites in Aquatic Species
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- Myxozoa, Cnidaria, evolutionary origin, phylogenomics, Myxobolus cerebralis, polar capsules, nematocysts, genome size reduction, gene enrichment analysis, genome assembly
- MeSH terms
- Animals, Phylogeny, Genome, Evolution, Molecular, Genomics, Polypodium, Myxobolus
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