Cited by 264Myxozoan Parasites in Aquatic SpeciesMarine Invertebrate Physiology and EcologyGenomics and Phylogenetic Studies

Genomic insights into the evolutionary origin of Myxozoa within Cnidaria

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Chang, E. Sally, Neuhof, Moran, Rubinstein, Nimrod D., Diamant, Arik, Philippe, Hervé, Huchon, Dorothée, Cartwright, Paulyn·2015·Proceedings of the National Academy of Sciences

Abstract

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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Crossref · 10.1073/pnas.1511468112

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  • While strong support for Ctenophora-sister may be obtained from phylogenomic datasets, our analysis suggests these results are caused by undetected systematic bias.

    “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]

    The citation is attached to the first clause, about strong phylogenomic support for Ctenophora as sister to other animals; the systematic-bias conclusion is the citing authors’ own. The Phylogenetic Position section reports strong support for relationships within Cnidaria, while the Figure 2 text lists Ctenophora without stating its position or support. Searches for Ctenophora-sister and its support found no decisive passage in our copy. (LLM, conf=0.72)

    Experimental — accuracy not yet measured
  • The topologies from Chang and Feuda are based on the same data set made up of 51,940 amino acid positions from 78 taxa representing a wide range of animals and 9 non-animal outgroups.

    “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.”
  • Porifera-sister generally emerges when site-specific differences in amino acid composition are modeled and distant outgroups (e.g., Fungi) are not included in the analyses.

    “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.”
  • Two key phylogenomic datasets that previously supported Ctenophora-sister (WhelanD20 and Chang) display strong heterogeneity in amino acid composition across sites and taxa.

    “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”

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Research works printed but not linked: 2

  1. Evans NM, Holder MT, Barbeitos MS, Okamura B, Cartwright P (2010) The phyloge- netic position of Myxozoa: Exploring conflicting signals in phylogenomic and ribo- somal datasets. Mol Biol Evol 27(12):2733-2746.
  2. Zhi-Liang H, Jie B, Reecy JM (2008) CateGOrizer: A web-based program to batch analyze gene ontology classification categories. Online J Bioinform 9(2):108-112.

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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)
Venue
Proceedings of the National Academy of Sciences
Published
2015-11-16
Volume
112
Issue
48
Pages
14912-14917
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
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
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 › Biochemistry, Genetics and Molecular Biology › Cancer Research › Myxozoan Parasites in Aquatic Species
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › 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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