Summary Background Trichoplax adhaerens is the best-known member of the Phylum Placozoa, one of the earliest-diverging metazoan phyla. It is a small disk-shaped animal that glides on surfaces in warm oceans to feed on algae. Prior anatomical studies of Trichoplax revealed that it has a simple three-layered organization with four somatic cell types. Results We reinvestigate the cellular organization of Trichoplax using advanced freezing and microscopy techniques to identify localize and count cells. Six somatic cell types are deployed in stereotyped positions. A thick ventral plate, comprising the majority of the cells, includes ciliated epithelial cells, newly identified lipophil cells packed with large lipid granules, and gland cells. Lipophils project deep into the interior where they alternate with regularly spaced fiber cells whose branches contact all other cell types, including cells of the dorsal and ventral epithelium. Crystal cells, each containing a birefringent crystal, are arrayed around the rim. Gland cells express several proteins typical of neurosecretory cells, and a subset of them, around the rim, also expresses an FMRFamide-like neuropeptide. Conclusions Structural analysis of Trichoplax with significantly improved techniques provides an advance in understanding its cell types and their distributions. We find two previously undetected cell types, lipohil and crystal cells, and an organized body plan in which different cell types are arranged in distinct patterns. The composition of gland cells suggests that they are neurosecretory cells and could control locomotor and feeding behavior.
For more than a century, the origin of metazoan animals has been debated. One aspect of this debate has been centered on what the hypothetical “urmetazoon” bauplan might have been. The morphologically most simply organized metazoan animal, the placozoan Trichoplax adhaerens, resembles an intriguing model for one of several “urmetazoon” hypotheses: the placula hypothesis. Clear support for a basal position of Placozoa would aid in resolving several key issues of metazoan-specific inventions (including, for example, head–foot axis, symmetry, and coelom) and would determine a root for unraveling their evolution. Unfortunately, the phylogenetic relationships at the base of Metazoa have been controversial because of conflicting phylogenetic scenarios generated while addressing the question. Here, we analyze the sum of morphological evidence, the secondary structure of mitochondrial ribosomal genes, and molecular sequence data from mitochondrial and nuclear genes that amass over 9,400 phylogenetically informative characters from 24 to 73 taxa. Together with mitochondrial DNA genome structure and sequence analyses and Hox-like gene expression patterns, these data (1) provide evidence that Placozoa are basal relative to all other diploblast phyla and (2) spark a modernized “urmetazoon” hypothesis.
The enigmatic animal phylum Placozoa holds a key position in the metazoan Tree of Life. A simple bauplan makes it appear to be the most basal metazoan known and genetic evidence also points to a position close to the last common metazoan ancestor. Trichoplax adhaerens is the only formally described species in the phylum to date, making the Placozoa the only monotypic phylum in the animal kingdom. However, recent molecular genetic as well as morphological studies have identified a high level of diversity, and hence a potential high level of taxonomic diversity, within this phylum. Different taxa, possibly at different taxonomic levels, are awaiting description. In this review we firstly summarize knowledge on the morphology, phylogenetic position and ecology of the Placozoa. Secondly, we give an overview of placozoan morphological and genetic diversity and finally present an updated distribution of placozoan populations. We conclude that there is great potential and need to erect new taxa and to establish a firm system for this taxonomic tabula rasa.
Bacterial symbionts are integral to the health and homeostasis of invertebrate hosts. Notably, members of the Rickettsiales genus Wolbachia influence several aspects of the fitness and evolution of their terrestrial hosts, but few analogous partnerships have been found in marine systems. We report here the genome, phylogenetics, and biogeography of a ubiquitous and novel Rickettsiales species that primarily associates with marine organisms. We previously showed that this bacterium was found in scleractinian corals, responds to nutrient exposure, and is associated with reduced host growth and increased mortality. This bacterium, like other Rickettsiales, has a reduced genome indicative of a parasitic lifestyle. Phylogenetic analysis places this Rickettsiales within a new genus we define as “Candidatus Aquarickettsia.” Using data from the Earth Microbiome Project and SRA databases, we also demonstrate that members of “Ca. Aquarickettsia” are found globally in dozens of invertebrate lineages. The coral-associated “Candidatus A. rohweri” is the first finished genome in this new clade. “Ca. A. rohweri” lacks genes to synthesize most sugars and amino acids but possesses several genes linked to pathogenicity including Tlc, an antiporter that exchanges host ATP for ADP, and a complete Type IV secretion system. Despite its inability to metabolize nitrogen, “Ca. A. rohweri” possesses the NtrY-NtrX two-component system involved in sensing and responding to extracellular nitrogen. Given these data, along with visualization of the parasite in host tissues, we hypothesize that “Ca. A. rohweri” reduces coral health by consuming host nutrients and energy, thus weakening and eventually killing host cells. Last, we hypothesize that nutrient enrichment, which is increasingly common on coral reefs, encourages unrestricted growth of “Ca. A. rohweri” in its host by providing abundant N-rich metabolites to be scavenged.
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.
Placozoa has been a key phylum for understanding early metazoan evolution. Yet this phylum is officially monotypic and with respect to its general biology and ecology has remained widely unknown. Worldwide sampling and sequencing of the mitochondrial large ribosomal subunit (16S) reveals a cosmopolitan distribution in tropical and subtropical waters of genetically different clades. We sampled a total of 39 tropical and subtropical locations worldwide and found 23 positive sites for placozoans. The number of genetically characterized sites was thereby increased from 15 to 37. The new sampling identified the first genotypes from two new oceanographic regions, the Eastern Atlantic and the Indian Ocean. We found seven out of 11 previously known haplotypes as well as five new haplotypes. One haplotype resembles a new genetic clade, increasing the number of clades from six to seven. Some of these clades seem to be cosmopolitan whereas others appear to be endemic. The phylogeography also shows that different clades occupy different ecological niches and identifies several euryoecious haplotypes with a cosmopolitic distribution as well as some stenoecious haplotypes with an endemic distribution. Haplotypes of different clades differ substantially in their phylogeographic distribution according to latitude. The genetic data also suggest deep phylogenetic branching patterns between clades.
Background: The membrane-associated progesterone receptor (MAPR) family consists of heme-binding proteins containing a cytochrome b5 (cytb5) domain characterized by the presence of a MAPR-specific interhelical insert region (MIHIR) between helices 3 and 4 of the canonical cytb5-domain fold. Animals possess three MAPR families (PGRMClike, Neuferricin and Neudesin). Results: Here we show that all animal MAPR families were already present in the common ancestor of the Opisthokonta (comprising animals and fungi as well as related protistan taxa). All three MAPR genes acquired extensions C-terminal to the cytb5 domain, either before or with the evolution of animals. The archetypical MAPR protein, progesterone receptor membrane component 1 (PGRMC1), contains phosphorylated tyrosines Y139 and Y180. The combination of Y139/Y180 appeared in the common ancestor of Cnidaria and bilaterally symmetrical animals, along with an early embryological organizer and synapsed neurons, and is strongly conserved in all bilateral animals. A predicted protein interaction motif in the PGRMC1 MIHIR is potentially regulated by Y139 phosphorylation. A multilayered model of animal MAPR function acquisition includes some pre-metazoan functions (e.g., heme binding and cytochrome P450 interactions) and some acquired animal-specific functions that involve regulation of strongly conserved protein interaction motifs acquired by early-branching animals. Conclusions: This study provides a conceptual framework for future studies, against which PGRMC1's multiple functions can perhaps be stratified and functionally dissected. In accompanying papers we show that mutational perturbation of PGRMC1 phosphorylation status of the Y180 motif is associated with dramatic changes cell pasticity assayed by protein abundances, cell morphology, mitochondrial function, genomic stability, and epigenetic status, with pathways analysis associating Y180 mutation with processes related to organizer function. These combined works reveal .
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