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Adamska, M.

Publications and source records attributed to Adamska, M..

4 recordsLinked to original sources

Calcareous sponge cell atlas provides support to homology between sponge and eumetazoan body plans

Sponges are widely recognized as important model organisms for studying animal evolution, due to their phylogenetic position at the base of the animal tree of life, as well as similarities to the nearest animal relatives, the choanoflagellates. A critical aspect of animal evolution concerns the origin of germ layers, the embryonic structures which give rise to all tissues and organs of animal bodies. Haeckels hypothesis suggested a germ layer homology between sponges and corals, and thus all eumetazoans (complex animals including cnidarians and bilaterians). According to this hypothesis, sponge choanoderm (composed of the feeding cells, choanocytes) and sponge pinacoderm (the outer epithelium) would be homologous to eumetazoan endoderm (from which the digestive system originates) and the ectoderm (giving rise to the epidermis), respectively. We addressed this hypothesis comparing tissue-specific transcriptomes derived from single-cell transcriptome datasets of sponges and cnidarians. We have sequenced single cell transcriptomes of Australian calcareous sponge, Sycon capricorn, and identified its cell types using a combination of in silico annotation of the cell clusters and in situ hybridization with marker genes. Single-cell transcriptome datasets for two demosponge species and two cnidarian species were extracted from recent literature. Homology was assessed using the SAMap algorithm, which has been designed to identify homologous cell types across vast evolutionary distances by detection of shared expression profiles. Our results are fully consistent with Haeckels hypothesis, supporting homology between the innermost layers of sponges and cnidarians (choanoderm and endoderm/gastrodermis) as well as the outermost layers of sponges and cnidarians (pinacoderm and ectoderm/epidermis). Thus, sponge body plan appears to represent an intermediate step between single cell protists (choanoflagellates) and complex animals, rather than being independent experiment in animal multicellularity as suggested by alternative hypotheses.

evolutionary biology↗

Body-plan reorganization in a sponge correlates with microbiome change

Mounting evidence suggests that animals and their associated bacteria interact via intricate molecular mechanisms, and it is hypothesized that disturbances to the microbiome can influence animal development. Sponges diverged from other animals more than 750 MYA and represent one of the earliest branching animal phyla that exhibit symbiotic relationships with diverse bacteria. Over 41 microbial phyla have been found in association with sponges, forming a holobiont that is integral to aquatic ecosystems worldwide. Sponge-associated microbes contain an enriched set of proteins bearing eukaryotic-like domains, and their metabolism supports the host with nutrients. This indicates strong physiological interconnections in the holobiont, which are thought to be modulated by sponge immunity and pattern-recognition proteins. Despite the hypothesized tight physiological integration and ancient origin of the sponge holobiont, the effect of changes in the symbiotic community on the sponge metabolism and morphogenesis remains poorly understood. Here, we show that the loss of a key microbial sponge symbiont correlates with a stark body plan reorganization of the sponge host. This reorganization is coupled with broad transcriptomic changes and includes the modulation of signaling pathways known to be involved in morphogenesis and innate immune response in sponges and other animals. This study provides a combined genetic, physiological, and morphological assessment of the effect of changes in the microbiome on sponge post-embryonic development and homeostasis. The drastic microbiome reorganization and the correlated response observed in the sponge host provide evidence for a coupling between sponge transcriptomic state and the state of its microbiome. Our results suggest that sponges use molecular mechanisms to respond to changes in their microbiome and that the ability to sense and respond to microbiome perturbations has deep evolutionary origins among animals.

genomics↗

Fast transcriptional activation of developmental signalling pathways during wound healing of the calcareous sponge Sycon ciliatum

BackgroundThe ability to regenerate lost or damaged body parts is an ancient animal characteristic with a wide yet variable distribution across all phyla. Sponges, likely the sister group to all other animals, have remarkable regenerative abilities including whole body regeneration and re-development from dissociated cells. The calcareous sponge Sycon ciliatum has been subject to various regeneration studies since the beginning of the last century. However, the early steps of wound healing of S. ciliatum have not been addressed from the molecular perspective. ResultsIn this study, we combined electron microscopy with gene expression analysis to investigate wound healing after transverse sectioning of S. ciliatum. Microscopic analysis revealed massive transdifferentiation and collective migration behaviour of choanocytes and pinacocytes early upon injury (6-12h) as the main mechanisms for quick closure of the wound surface. RNA-sequencing identified upregulation of components of the conserved metazoan Wnt and TGF{beta} signalling pathways within 3h, preceding morphologically detectable wound healing events. De novo upregulation after a decline in expression coincides with morphologically visible polarity establishment. Moreover, by integrating the new wound healing data set with previously published data derived from intact sponge, we demonstrate similarity between gene activity during early wound healing and osculum maintenance. Whole mount in situ hybridisation of the TGF{beta} signalling pathway ligand SciTGF{beta}U and signal transducer SciSmadRa show that the early activation of both is initially encompassing a large area surrounding the cut surface with gradual restriction to the edge of the forming regenerative membrane as wound healing progresses. While SciTGF{beta}U transcripts are localised to exo- and endopinacocytes, SciSmadRa expression appears across all cell types. Using an EdU cell proliferation assay, we found that a global increase in cell proliferation is not visible before 12h into wound healing. Hence, the initial stages to cover the injury site including cell transdifferentiation and migration seem to be executed by cells remaining after injury. Gene expression clustering coupled with GO term enrichment analysis confirmed that expression of genes involved in processes related to cell proliferation, DNA repair as well as apoptotic processes at 3 and 6h of wound healing was not upregulated. On the other hand, genes associated with positive regulation of transcription, signal transduction, actin filament and chromatin organisation, as well as the Wnt signalling pathway are upregulated at early wound healing stages. ConclusionWe have analysed wound healing in the calcareous sponge Sycon ciliatum using microscopic and genomic methods. This study highlights a remarkable mechanism of interplay between cell transdifferentiation and collective migration we hypothesise to be regulated by conserved metazoan developmental pathways and numerous taxonomically restricted genes. Expression of these genes in regenerating and intact sponges sheds light on the long-standing question whether embryonic developmental pathways are redeployed in regeneration.

developmental biology↗

The role of homology and orthology in the phylogenomic analysis of metazoan gene content

Resolving animal (Metazoa) relationships is crucial to our understanding of, for example, the origin of their key traits such as muscles, guts and nerves. However, a broadly accepted metazoan consensus phylogeny has yet to emerge. In part this is because the genomes of deeply-diverging and fast-evolving lineages may undergo significant gene turnover, reducing the number of orthologs shared with related phyla. This can limit the usefulness of traditional phylogenetic methods that rely on alignments of orthologous sequences. Phylogenetic analysis of gene content has the potential to circumvent this orthology requirement, with binary presence/absence of homologous gene families representing a source of phylogenetically informative characters. Applying binary substitution models to the gene content of 26 complete animal genomes, we demonstrate that patterns of gene conservation differ markedly depending on whether gene families are defined by orthology or homology, i.e., whether paralogs are excluded or included. We conclude that the placement of deeply-diverging lineages, like ctenophores, may exceed the limit of resolution afforded by methods based on comparisons of orthologous protein supermatrices, and novel approaches are required to fully capture the evolutionary signal from genes within genomes.

evolutionary biology↗