Comparative genomics and the nature of placozoan species

Bibliographic Details
Title: Comparative genomics and the nature of placozoan species
Authors: Warren R. Francis, Bernd Schierwater, Helmut Blum, Gert Wörheide, Stefan Krebs, Michael Eitel, Sergio Vargas, Jean Daraspe, Gray A. Williams, Frederique Varoqueaux, Hans-Jürgen Osigus
Source: PLoS Biology
PLOS Biology
PLoS Biology, Vol 16, Iss 7, p e2005359 (2018)
PLoS biology, vol. 16, no. 7, pp. e2005359
Publisher Information: Public Library of Science (PLoS), 2018.
Publication Year: 2018
Subject Terms: General Agricultural and Biological Sciences, General Immunology and Microbiology, General Biochemistry, Genetics and Molecular Biology, General Neuroscience, Phylogenetics, Genetic diversity, Genomics, Phylum, Placozoa, biology.organism_classification, biology, Trichoplax, Comparative genomics, Genetic Speciation, Evolutionary biology, Short Reports, Biology and Life Sciences, Organisms, Eukaryota, Animals, Invertebrates, Trichoplax Adhaerens, Research and Analysis Methods, Database and Informatics Methods, Bioinformatics, Sequence Analysis, Sequence Alignment, Computational Biology, Comparative Genomics, Genetics, Evolutionary Biology, Evolutionary Systematics, Phylogenetic Analysis, Taxonomy, Computer and Information Sciences, Data Management, Cnidaria, Biochemistry, Bioenergetics, Energy-Producing Organelles, Mitochondria, Cell Biology, Cellular Structures and Organelles, ddc:550, ddc:540, Department für Geo- und Umweltwissenschaften, Department Biochemie, Biology (General), QH301-705.5, Alleles, Base Sequence, DNA, Ribosomal/genetics, Gene Duplication, Gene Rearrangement/genetics, Genetic Variation, Genome, Molecular Sequence Annotation, Phylogeny, Placozoa/genetics, Placozoa/ultrastructure, Reproductive Isolation, Correction
Description: Placozoans are a phylum of nonbilaterian marine animals currently represented by a single described species, Trichoplax adhaerens, Schulze 1883. Placozoans arguably show the simplest animal morphology, which is identical among isolates collected worldwide, despite an apparently sizeable genetic diversity within the phylum. Here, we use a comparative genomics approach for a deeper appreciation of the structure and causes of the deeply diverging lineages in the Placozoa. We generated a high-quality draft genome of the genetic lineage H13 isolated from Hong Kong and compared it to the distantly related T. adhaerens. We uncovered substantial structural differences between the two genomes that point to a deep genomic separation and provide support that adaptation by gene duplication is likely a crucial mechanism in placozoan speciation. We further provide genetic evidence for reproductively isolated species and suggest a genus-level difference of H13 to T. adhaerens, justifying the designation of H13 as a new species, Hoilungia hongkongensis nov. gen., nov. spec., now the second described placozoan species and the first in a new genus. Our multilevel comparative genomics approach is, therefore, likely to prove valuable for species distinctions in other cryptic microscopic animal groups that lack diagnostic morphological characters, such as some nematodes, copepods, rotifers, or mites.
Author summary Placozoans are a phylum of tiny (approximately 1 mm) marine animals that are found worldwide in temperate and tropical waters. They are characterized by morphological simplicity, with only a handful of cell types, no neurons, no tissue organization, and even no axial polarity. Since the original description of Trichoplax adhaerens 135 years ago, no additional accepted species has been established, leaving the Placozoa as the only animal phylum with only a single formally described species. While classical morphological species identification has failed to reveal further species, single-gene DNA sequence analyses have identified a broad and deep genetic diversity within the Placozoa. To address the significance of this deep genetic diversity in this morphologically uniform phylum, and to better understand its consequences for speciation processes, general biology, and species delimitation in the Placozoa, we sequenced the genome of the placozoan isolate “H13,” a lineage distantly genetically related to T. adhaerens. Our multilevel genomic comparisons with the T. adhaerens genome show considerable differences in the general structure of the genome and the makeup and history of various gene families of biological relevance to habitat adaptation. Based on comparative genomics, we here describe the second placozoan species and show that it belongs to a new genus.
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