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Bernd Schierwater - One of the best experts on this subject based on the ideXlab platform.
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Innate immunity in the simplest animals – Placozoans
BMC, 2019Co-Authors: Kai Kamm, Bernd Schierwater, Rob DesalleAbstract:Abstract Background Innate immunity provides the core recognition system in animals for preventing infection, but also plays an important role in managing the relationship between an animal host and its symbiont. Most of our knowledge about innate immunity stems from a few animal model systems, but substantial variation between metazoan phyla has been revealed by comparative genomic studies. The exploration of more taxa is still needed to better understand the evolution of immunity related mechanisms. Placozoans are morphologically the simplest organized metazoans and the association between these enigmatic animals and their rickettsial endosymbionts has recently been elucidated. Our analyses of the novel Placozoan nuclear genome of Trichoplax sp. H2 and its associated rickettsial endosymbiont genome clearly pointed to a mutualistic and co-evolutionary relationship. This discovery raises the question of how the Placozoan holobiont manages symbiosis and, conversely, how it defends against harmful microorganisms. In this study, we examined the annotated genome of Trichoplax sp. H2 for the presence of genes involved in innate immune recognition and downstream signaling. Results A rich repertoire of genes belonging to the Toll-like and NOD-like receptor pathways, to scavenger receptors and to secreted fibrinogen-related domain genes was identified in the genome of Trichoplax sp. H2. Nevertheless, the innate immunity related pathways in Placozoans deviate in several instances from well investigated vertebrates and invertebrates. While true Toll- and NOD-like receptors are absent, the presence of many genes of the downstream signaling cascade suggests at least primordial Toll-like receptor signaling in Placozoa. An abundance of scavenger receptors, fibrinogen-related domain genes and Apaf-1 genes clearly constitutes an expansion of the immunity related gene repertoire specific to Placozoa. Conclusions The found wealth of immunity related genes present in Placozoa is surprising and quite striking in light of the extremely simple Placozoan body plan and their sparse cell type makeup. Research is warranted to reveal how Placozoa utilize this immune repertoire to manage and maintain their associated microbiota as well as to fend-off pathogens
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high cell diversity and complex peptidergic signaling underlie Placozoan behavior
Current Biology, 2018Co-Authors: Frédérique Varoqueaux, Kai Kamm, Bernd Schierwater, E Williams, Susie Grandemange, Luca Truscello, Gaspar Jekely, Dirk FasshauerAbstract:Placozoans, together with sponges, are the only animals devoid of a nervous system and muscles, yet both respond to sensory stimulation in a coordinated manner. How behavioral control in these free-living animals is achieved in the absence of neurons and, more fundamentally, how the first neurons evolved from more primitive cells for communication during the rise of animals are not yet understood [1-5]. The Placozoan Trichoplax adhaerens is a millimeter-wide, flat, free-living marine animal composed of six morphologically identified cell types distributed across a simple body plan [6-9]: a thin upper epithelium and a columnar lower epithelium interspersed with a loose layer of fiber cells in between. Its genome contains genes encoding several neuropeptide-precursor-like proteins and orthologs of proteins involved in neurosecretion in animals with a nervous system [10-12]. Here we investigate peptidergic signaling in T. adhaerens. We found specific expression of several neuropeptide-like molecules in non-overlapping cell populations distributed over the three cell layers, revealing an unsuspected cell-type diversity of T. adhaerens. Using live imaging, we discovered that treatments with 11 different peptides elicited striking and consistent effects on the animals' shape, patterns of movement, and velocity that we categorized under three main types: (1) crinkling, (2) turning, and (3) flattening and churning. Together, the data demonstrate a crucial role for peptidergic signaling in nerveless Placozoans and suggest that peptidergic volume signaling may have pre-dated synaptic signaling in the evolution of nervous systems.
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Comparative genomics and the nature of Placozoan species.
PLoS biology, 2018Co-Authors: Michael Eitel, Hans-jürgen Osigus, Warren R. Francis, Frédérique Varoqueaux, Jean Daraspe, Stefan Krebs, Sergio Vargas, Helmut Blum, Gray A. Williams, Bernd SchierwaterAbstract: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.
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Trichoplax genomes reveal profound admixture and suggest stable wild populations without bisexual reproduction.
Scientific reports, 2018Co-Authors: Kai Kamm, Peter F. Stadler, Hans-jürgen Osigus, Rob Desalle, Bernd SchierwaterAbstract:The phylum Placozoa officially consists of only a single described species, Trichoplax adhaerens, although several lineages can be separated by molecular markers, geographical distributions and environmental demands. The Placozoan 16S haplotype H2 (Trichoplax sp. H2) is the most robust and cosmopolitan lineage of Placozoans found to date. In this study, its genome was found to be distinct but highly related to the Trichoplax adhaerens reference genome, for remarkably unique reasons. The pattern of variation and allele distribution between the two lineages suggests that both originate from a single interbreeding event in the wild, dating back at least several decades ago, and both seem not to have engaged in sexual reproduction since. We conclude that populations of certain Placozoan haplotypes remain stable for long periods without bisexual reproduction. Furthermore, allelic variation within and between the two Trichoplax lineages indicates that successful bisexual reproduction between related Placozoan lineages might serve to either counter accumulated negative somatic mutations or to cope with changing environmental conditions. On the other hand, enrichment of neutral or beneficial somatic mutations by vegetative reproduction, combined with rare sexual reproduction, could instantaneously boost genetic variation, generating novel ecotypes and eventually species.
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CM highlighting reproductive isolation between clades and a split into two genera.
2018Co-Authors: Michael Eitel, Hans-jürgen Osigus, Warren R. Francis, Frédérique Varoqueaux, Jean Daraspe, Stefan Krebs, Sergio Vargas, Helmut Blum, Gray A. Williams, Bernd SchierwaterAbstract:The CM for three nuclear-encoded ribosomal proteins (rpl9, rpl32, and rpp1) was generated by calculating (for each pair of isolates) the number of markers supporting their conspecificity in haploweb analyses (i.e., different individuals can be assigned to one species by shared alleles) minus the number of markers supporting the premise that they belong to different species. The CM was visualized as a heat map with different colors representing various amounts of shared alleles from −3 (no shared alleles) to +3 (3 shared alleles). Higher scores (red), therefore, indicate conspecific isolates, while gray tones support reproductive isolation, i.e., separate biological species. The number of sequenced markers per isolate is given in brackets beside the isolate (see S6 Table for details on isolates). The CM shows that allele sharing can occur between haplotypes within but never between clades. This is the first evidence for reproductive isolation between Placozoan clades and the first molecular support for the existence of biological species in the Placozoa. The CM furthermore supports the phylogenetic split between Trichoplax (clade I; note: no data available for clade II) and the new Placozoan genus Hoilungia (clades III–VII), as shown in the dendrogram on top of the heatmap. These clades are consistent with those recovered from analyses of the mitochondrial ribosomal large subunit (16S) [5] and compensatory base changes in the ITS2 [55]. Data underlying this figure can be found at https://bitbucket.org/molpalmuc/hoilungia-genome/src/master/reproductive_isolation/. CM, conspecificity matrix; ITS2, internal transcribed spacer 2.
Joseph F. Ryan - One of the best experts on this subject based on the ideXlab platform.
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dorsal ventral genes are part of an ancient axial patterning system evidence from trichoplax adhaerens Placozoa
Molecular Biology and Evolution, 2019Co-Authors: Joseph F. Ryan, Timothy Q. Dubuc, Mark Q. MartindaleAbstract:Placozoa are a morphologically simplistic group of marine animals found globally in tropical and subtropical environments. They consist of two named species, Trichoplax adhaerens and more recently Hoilungia hongkongensis, both with roughly six morphologically distinct cell types. With a sequenced genome, a limited number of cell types, and a simple flattened morphology, Trichoplax is an ideal model organism from which to explore the biology of an animal with a cellular complexity analagous to that of the earliest animals. Using a new approach for identification of gene expression patterns, this research looks at the relationship of Chordin/TgfΒ signaling and the axial patterning system of Placozoa. Our results suggest that Placozoans have an oral-aboral axis similar to cnidarians and that the parahoxozoan ancestor (common ancestor of Placozoa and Cnidaria) was likely radially symmetric.
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The radial expression of dorsal-ventral patterning genes in Placozoans, Trichoplax adhaerens, argues for an oral-aboral axis
2018Co-Authors: Timothy Q. Dubuc, Yuriy V. Bobkov, Joseph F. RyanAbstract:The Placozoans are a morphologically simplistic group of marine animals found globally in tropical and subtropical environments. They consist of a single named species, Trichoplax adhaerens and have roughly six morphologically distinct cell types. With a sequenced genome, a limited number of cell-types and a simple flattened morphology, Trichoplax is an ideal model organism to understand cellular dynamics and tissue patterning in the first animals. Using new approaches for identification of gene expression patterns this research looks at the relationship of Chordin/Tgfβ signaling and the axial patterning system of Placozoa. Our results suggest that Placozoans have an oral-aboral axis similar to cnidarians and that the parahoxozoan ancestor (common ancestor of Placozoa and Cnidaria) was likely radially symmetric.
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MicroRNAs and essential components of the microRNA processing machinery are not encoded in the genome of the ctenophore Mnemiopsis leidyi
BMC Genomics, 2012Co-Authors: Evan K. Maxwell, Christine E Schnitzler, Joseph F. Ryan, William E. Browne, Athanasios D. BaxevanisAbstract:Background: MicroRNAs play a vital role in the regulation of gene expression and have been identified in every animal with a sequenced genome examined thus far, except for the Placozoan Trichoplax. The genomic repertoires of metazoan microRNAs have become increasingly endorsed as phylogenetic characters and drivers of biological complexity. Results: In this study, we report the first investigation of microRNAs in a species from the phylum Ctenophora. We use short RNA sequencing and the assembled genome of the lobate ctenophore Mnemiopsis leidyi to show that this species appears to lack any recognizable microRNAs, as well as the nuclear proteins Drosha and Pasha, which are critical to canonical microRNA biogenesis. This finding represents the first reported case of a metazoan lacking a Drosha protein. Conclusions: Recent phylogenomic analyses suggest that Mnemiopsis may be the earliest branching metazoan lineage. If this is true, then the origins of canonical microRNA biogenesis and microRNA-mediated gene regulation may postdate the last common metazoan ancestor. Alternatively, canonical microRNA functionality may have been lost independently in the lineages leading to both Mnemiopsis and the Placozoan Trichoplax, suggesting that microRNA functionality was not critical until much later in metazoan evolution.
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micrornas and essential components of the microrna processing machinery are not encoded in the genome of the ctenophore mnemiopsis leidyi
BMC Genomics, 2012Co-Authors: Christine E Schnitzler, Joseph F. Ryan, William E. Browne, Evan Maxwell, Athanasios D. BaxevanisAbstract:MicroRNAs play a vital role in the regulation of gene expression and have been identified in every animal with a sequenced genome examined thus far, except for the Placozoan Trichoplax. The genomic repertoires of metazoan microRNAs have become increasingly endorsed as phylogenetic characters and drivers of biological complexity. In this study, we report the first investigation of microRNAs in a species from the phylum Ctenophora. We use short RNA sequencing and the assembled genome of the lobate ctenophore Mnemiopsis leidyi to show that this species appears to lack any recognizable microRNAs, as well as the nuclear proteins Drosha and Pasha, which are critical to canonical microRNA biogenesis. This finding represents the first reported case of a metazoan lacking a Drosha protein. Recent phylogenomic analyses suggest that Mnemiopsis may be the earliest branching metazoan lineage. If this is true, then the origins of canonical microRNA biogenesis and microRNA-mediated gene regulation may postdate the last common metazoan ancestor. Alternatively, canonical microRNA functionality may have been lost independently in the lineages leading to both Mnemiopsis and the Placozoan Trichoplax, suggesting that microRNA functionality was not critical until much later in metazoan evolution.
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Origin of LIM classes and families.
2012Co-Authors: Bernard J Koch, Joseph F. Ryan, Athanasios D. BaxevanisAbstract:Arrows indicate the stem lineage where a particular group of LIM proteins originated. Classes are denoted in capital letters and are not shown in parentheses. Families are denoted in lower case and appear after the class. The first appearance of a class is in red, while subsequent appearances of families of that class are in blue. The tree is based on the ParaHoxozoa hypothesis [109]. The phyla represented are as follows: Capsaspora ocwazarki (Filasterea), Salpingoeca rosetta (Choanoflagellatea), Monosiga brevicollis (Choanoflagellatea), Amphimedon queenslandica (Porifera), Mnemiopsis leidyi (Ctenophora), Nematostella vectensis (Cnidaria), Trichoplax adhaerens (Placozoa), Drosophila melanogaster (Arthropoda), and Homo sapiens (Vertebrata).
Rob Desalle - One of the best experts on this subject based on the ideXlab platform.
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Innate immunity in the simplest animals – Placozoans
BMC, 2019Co-Authors: Kai Kamm, Bernd Schierwater, Rob DesalleAbstract:Abstract Background Innate immunity provides the core recognition system in animals for preventing infection, but also plays an important role in managing the relationship between an animal host and its symbiont. Most of our knowledge about innate immunity stems from a few animal model systems, but substantial variation between metazoan phyla has been revealed by comparative genomic studies. The exploration of more taxa is still needed to better understand the evolution of immunity related mechanisms. Placozoans are morphologically the simplest organized metazoans and the association between these enigmatic animals and their rickettsial endosymbionts has recently been elucidated. Our analyses of the novel Placozoan nuclear genome of Trichoplax sp. H2 and its associated rickettsial endosymbiont genome clearly pointed to a mutualistic and co-evolutionary relationship. This discovery raises the question of how the Placozoan holobiont manages symbiosis and, conversely, how it defends against harmful microorganisms. In this study, we examined the annotated genome of Trichoplax sp. H2 for the presence of genes involved in innate immune recognition and downstream signaling. Results A rich repertoire of genes belonging to the Toll-like and NOD-like receptor pathways, to scavenger receptors and to secreted fibrinogen-related domain genes was identified in the genome of Trichoplax sp. H2. Nevertheless, the innate immunity related pathways in Placozoans deviate in several instances from well investigated vertebrates and invertebrates. While true Toll- and NOD-like receptors are absent, the presence of many genes of the downstream signaling cascade suggests at least primordial Toll-like receptor signaling in Placozoa. An abundance of scavenger receptors, fibrinogen-related domain genes and Apaf-1 genes clearly constitutes an expansion of the immunity related gene repertoire specific to Placozoa. Conclusions The found wealth of immunity related genes present in Placozoa is surprising and quite striking in light of the extremely simple Placozoan body plan and their sparse cell type makeup. Research is warranted to reveal how Placozoa utilize this immune repertoire to manage and maintain their associated microbiota as well as to fend-off pathogens
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Trichoplax genomes reveal profound admixture and suggest stable wild populations without bisexual reproduction.
Scientific reports, 2018Co-Authors: Kai Kamm, Peter F. Stadler, Hans-jürgen Osigus, Rob Desalle, Bernd SchierwaterAbstract:The phylum Placozoa officially consists of only a single described species, Trichoplax adhaerens, although several lineages can be separated by molecular markers, geographical distributions and environmental demands. The Placozoan 16S haplotype H2 (Trichoplax sp. H2) is the most robust and cosmopolitan lineage of Placozoans found to date. In this study, its genome was found to be distinct but highly related to the Trichoplax adhaerens reference genome, for remarkably unique reasons. The pattern of variation and allele distribution between the two lineages suggests that both originate from a single interbreeding event in the wild, dating back at least several decades ago, and both seem not to have engaged in sexual reproduction since. We conclude that populations of certain Placozoan haplotypes remain stable for long periods without bisexual reproduction. Furthermore, allelic variation within and between the two Trichoplax lineages indicates that successful bisexual reproduction between related Placozoan lineages might serve to either counter accumulated negative somatic mutations or to cope with changing environmental conditions. On the other hand, enrichment of neutral or beneficial somatic mutations by vegetative reproduction, combined with rare sexual reproduction, could instantaneously boost genetic variation, generating novel ecotypes and eventually species.
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2015Co-Authors: Bernd Schierwater, Wolfgang Jakob, Michael Eitel, Stephen L Dellaporta, Heike Hadrys, Sergios-orestis Kolokotronis, Rob DesalleAbstract: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
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670 Can we ever identify the Urmetazoan?
2014Co-Authors: Bernd Schierwater, Rob DesalleAbstract:Synopsis Unraveling the root of the metazoan tree of life has been a difficult task since the time of Haeckel and the invention of phylogenetics. Even considerable amounts of recent molecular data have not provided a generally accepted answer. Here, we review the major problems of this phylogenetic conundrum and provide some directions for solving it. The ever lingering question: ‘‘What did the Urmetazoan look like?’ ’ has not lost its charm, appeal or elusiveness for one and a half centuries. A solid amount of organismal data give what some feel is a clear answer (e.g., Placozoa are at the base of the metazoan tree of life), a single ‘‘eye-catching’’ character gives an another appealing answer (e.g., Porifera at the base), and a diversity of molecular data gives almost as many answers as there are exemplars, and recent molecular analyses with large data sets even suggest that we may never be able t
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Global Diversity of the Placozoa
PloS one, 2013Co-Authors: Michael Eitel, Hans-jürgen Osigus, Rob DesalleAbstract: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.
Michael Eitel - One of the best experts on this subject based on the ideXlab platform.
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Comparative genomics and the nature of Placozoan species.
PLoS biology, 2018Co-Authors: Michael Eitel, Hans-jürgen Osigus, Warren R. Francis, Frédérique Varoqueaux, Jean Daraspe, Stefan Krebs, Sergio Vargas, Helmut Blum, Gray A. Williams, Bernd SchierwaterAbstract: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.
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CM highlighting reproductive isolation between clades and a split into two genera.
2018Co-Authors: Michael Eitel, Hans-jürgen Osigus, Warren R. Francis, Frédérique Varoqueaux, Jean Daraspe, Stefan Krebs, Sergio Vargas, Helmut Blum, Gray A. Williams, Bernd SchierwaterAbstract:The CM for three nuclear-encoded ribosomal proteins (rpl9, rpl32, and rpp1) was generated by calculating (for each pair of isolates) the number of markers supporting their conspecificity in haploweb analyses (i.e., different individuals can be assigned to one species by shared alleles) minus the number of markers supporting the premise that they belong to different species. The CM was visualized as a heat map with different colors representing various amounts of shared alleles from −3 (no shared alleles) to +3 (3 shared alleles). Higher scores (red), therefore, indicate conspecific isolates, while gray tones support reproductive isolation, i.e., separate biological species. The number of sequenced markers per isolate is given in brackets beside the isolate (see S6 Table for details on isolates). The CM shows that allele sharing can occur between haplotypes within but never between clades. This is the first evidence for reproductive isolation between Placozoan clades and the first molecular support for the existence of biological species in the Placozoa. The CM furthermore supports the phylogenetic split between Trichoplax (clade I; note: no data available for clade II) and the new Placozoan genus Hoilungia (clades III–VII), as shown in the dendrogram on top of the heatmap. These clades are consistent with those recovered from analyses of the mitochondrial ribosomal large subunit (16S) [5] and compensatory base changes in the ITS2 [55]. Data underlying this figure can be found at https://bitbucket.org/molpalmuc/hoilungia-genome/src/master/reproductive_isolation/. CM, conspecificity matrix; ITS2, internal transcribed spacer 2.
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Deep RNA sequencing reveals the smallest known mitochondrial micro exon in animals: The Placozoan cox1 single base pair exon.
PloS one, 2017Co-Authors: Hans-jürgen Osigus, Michael Eitel, Bernd SchierwaterAbstract:The phylum Placozoa holds a key position for our understanding of the evolution of mitochondrial genomes in Metazoa. Placozoans possess large mitochondrial genomes which harbor several remarkable characteristics such as a fragmented cox1 gene and trans-splicing cox1 introns. A previous study also suggested the existence of cox1 mRNA editing in Trichoplax adhaerens, yet the only formally described species in the phylum Placozoa. We have analyzed RNA-seq data of the undescribed sister species, Placozoa sp. H2 ("Panama" clone), with special focus on the mitochondrial mRNA. While we did not find support for a previously postulated cox1 mRNA editing mechanism, we surprisingly found two independent transcripts representing intermediate cox1 mRNA splicing stages. Both transcripts consist of partial cox1 exon as well as overlapping intron fragments. The data suggest that the cox1 gene harbors a single base pair (cytosine) micro exon. Furthermore, conserved group I intron structures flank this unique micro exon also in other Placozoans. We discuss the evolutionary origin of this micro exon in the context of a self-splicing intron gain in the cox1 gene of the last common ancestor of extant Placozoans.
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Comparison of Placozoan cox1 annotations.
2017Co-Authors: Hans-jürgen Osigus, Michael Eitel, Bernd SchierwaterAbstract:A) Positions and lengths of cox1 exons in Trichoplax adhaerens according to Burger et al. 2009 (NC_008151.2). B) Differences in numbering, position and length of cox1 exons in Trichoplax adhaerens considering the micro exon. C) Different positions of the cox1 micro exon in all known Placozoan mitochondrial genomes.
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Placozoan cox1 “micro exon” scenario.
2017Co-Authors: Hans-jürgen Osigus, Michael Eitel, Bernd SchierwaterAbstract:The scenario is based on Placozoa sp. H2 “Panama” RNA-seq data. Exon/intron color codes are the same as in Fig 2. Exon 61 represents a truncated exon 6 (following Burger et al., 2009), which is indicated by the superscript 1. Subsequent exons/introns also differ in boundaries and/or numbering from the annotation by Burger et al., 2009 (likewise indicated by a superscript 1). The former intron 6 is now split into two introns (intron 61 and 71, respectively) flanking the newly identified micro exon 71, which has been identified in this study. Splicing of exon 61, micro exon 71 and exon 81 (formerly exon 7, Burger et al., 2009) leads to an in-frame coding sequence (CDS) with the intact CAT triplet coding for the functionally indispensable histidine at the respective position.
Hans-jürgen Osigus - One of the best experts on this subject based on the ideXlab platform.
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Comparative genomics and the nature of Placozoan species.
PLoS biology, 2018Co-Authors: Michael Eitel, Hans-jürgen Osigus, Warren R. Francis, Frédérique Varoqueaux, Jean Daraspe, Stefan Krebs, Sergio Vargas, Helmut Blum, Gray A. Williams, Bernd SchierwaterAbstract: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.
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Trichoplax genomes reveal profound admixture and suggest stable wild populations without bisexual reproduction.
Scientific reports, 2018Co-Authors: Kai Kamm, Peter F. Stadler, Hans-jürgen Osigus, Rob Desalle, Bernd SchierwaterAbstract:The phylum Placozoa officially consists of only a single described species, Trichoplax adhaerens, although several lineages can be separated by molecular markers, geographical distributions and environmental demands. The Placozoan 16S haplotype H2 (Trichoplax sp. H2) is the most robust and cosmopolitan lineage of Placozoans found to date. In this study, its genome was found to be distinct but highly related to the Trichoplax adhaerens reference genome, for remarkably unique reasons. The pattern of variation and allele distribution between the two lineages suggests that both originate from a single interbreeding event in the wild, dating back at least several decades ago, and both seem not to have engaged in sexual reproduction since. We conclude that populations of certain Placozoan haplotypes remain stable for long periods without bisexual reproduction. Furthermore, allelic variation within and between the two Trichoplax lineages indicates that successful bisexual reproduction between related Placozoan lineages might serve to either counter accumulated negative somatic mutations or to cope with changing environmental conditions. On the other hand, enrichment of neutral or beneficial somatic mutations by vegetative reproduction, combined with rare sexual reproduction, could instantaneously boost genetic variation, generating novel ecotypes and eventually species.
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CM highlighting reproductive isolation between clades and a split into two genera.
2018Co-Authors: Michael Eitel, Hans-jürgen Osigus, Warren R. Francis, Frédérique Varoqueaux, Jean Daraspe, Stefan Krebs, Sergio Vargas, Helmut Blum, Gray A. Williams, Bernd SchierwaterAbstract:The CM for three nuclear-encoded ribosomal proteins (rpl9, rpl32, and rpp1) was generated by calculating (for each pair of isolates) the number of markers supporting their conspecificity in haploweb analyses (i.e., different individuals can be assigned to one species by shared alleles) minus the number of markers supporting the premise that they belong to different species. The CM was visualized as a heat map with different colors representing various amounts of shared alleles from −3 (no shared alleles) to +3 (3 shared alleles). Higher scores (red), therefore, indicate conspecific isolates, while gray tones support reproductive isolation, i.e., separate biological species. The number of sequenced markers per isolate is given in brackets beside the isolate (see S6 Table for details on isolates). The CM shows that allele sharing can occur between haplotypes within but never between clades. This is the first evidence for reproductive isolation between Placozoan clades and the first molecular support for the existence of biological species in the Placozoa. The CM furthermore supports the phylogenetic split between Trichoplax (clade I; note: no data available for clade II) and the new Placozoan genus Hoilungia (clades III–VII), as shown in the dendrogram on top of the heatmap. These clades are consistent with those recovered from analyses of the mitochondrial ribosomal large subunit (16S) [5] and compensatory base changes in the ITS2 [55]. Data underlying this figure can be found at https://bitbucket.org/molpalmuc/hoilungia-genome/src/master/reproductive_isolation/. CM, conspecificity matrix; ITS2, internal transcribed spacer 2.
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Deep RNA sequencing reveals the smallest known mitochondrial micro exon in animals: The Placozoan cox1 single base pair exon.
PloS one, 2017Co-Authors: Hans-jürgen Osigus, Michael Eitel, Bernd SchierwaterAbstract:The phylum Placozoa holds a key position for our understanding of the evolution of mitochondrial genomes in Metazoa. Placozoans possess large mitochondrial genomes which harbor several remarkable characteristics such as a fragmented cox1 gene and trans-splicing cox1 introns. A previous study also suggested the existence of cox1 mRNA editing in Trichoplax adhaerens, yet the only formally described species in the phylum Placozoa. We have analyzed RNA-seq data of the undescribed sister species, Placozoa sp. H2 ("Panama" clone), with special focus on the mitochondrial mRNA. While we did not find support for a previously postulated cox1 mRNA editing mechanism, we surprisingly found two independent transcripts representing intermediate cox1 mRNA splicing stages. Both transcripts consist of partial cox1 exon as well as overlapping intron fragments. The data suggest that the cox1 gene harbors a single base pair (cytosine) micro exon. Furthermore, conserved group I intron structures flank this unique micro exon also in other Placozoans. We discuss the evolutionary origin of this micro exon in the context of a self-splicing intron gain in the cox1 gene of the last common ancestor of extant Placozoans.
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Comparison of Placozoan cox1 annotations.
2017Co-Authors: Hans-jürgen Osigus, Michael Eitel, Bernd SchierwaterAbstract:A) Positions and lengths of cox1 exons in Trichoplax adhaerens according to Burger et al. 2009 (NC_008151.2). B) Differences in numbering, position and length of cox1 exons in Trichoplax adhaerens considering the micro exon. C) Different positions of the cox1 micro exon in all known Placozoan mitochondrial genomes.
