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Wörheide, G.

Publications and source records attributed to Wörheide, G..

14 recordsLinked to original sources

Genetic parallels in biomineralization of the calcareous sponge Sycon ciliatum and stony corals

The rapid emergence of mineralized structures in diverse animal groups during the late Ediacaran and early Cambrian periods likely resulted from modifications of pre-adapted biomineralization genes inherited from a common ancestor. As the oldest extant phylum with mineralized structures, sponges are key to understanding animal biomineralization. Yet, the biomineralization process in sponges, particularly in forming spicules, is not well-understood. To address this, we conducted transcriptomic, genomic, and proteomic analyses on the calcareous sponge Sycon ciliatum, supplemented by in situ hybridization. We identified 829 genes overexpressed in regions of increased calcite spicule formation, including 17 calcarins--proteins analogous to corals galaxins localized in the spicule matrix and expressed in sclerocytes. Their expression varied temporally and spatially, specific to certain spicule types, indicating that fine-tuned gene regulation is crucial for biomineralization control. Similar subtle expression changes are also relevant in stony coral biomineralization. Tandem gene arrangements and expression changes suggest that gene duplication and neofunctionalization have significantly shaped Sycon ciliatums biomineralization, similar to that in corals. These findings suggest a parallel evolution of carbonate biomineralization in the calcitic Sycon ciliatum and aragonitic corals, exemplifying the evolution of mechanisms crucial for animals to act as ecosystem engineers and form reef structures.

evolutionary biology↗

Barcoding-inferred biodiversity of shallow-water Indo-Pacific demosponges

AimThe Indo-Pacific is the worlds largest marine biogeographic region. It is characterised by different degrees of connectivity among its subregions, and harbours the majority of demosponge species currently known to science. Comparisons between several regional sponge faunas have been undertaken in the past, mostly based on identifying the sponge species morphologically. The Sponge Barcoding Project, in tandem with other regional DNA taxonomy campaigns, provides one of the largest DNA-based taxonomic data collections from sponges of the Indo-Pacific. Here, we utilise the sponge barcoding data in the largest molecular biodiversity study of sponges to date, which reveals patterns of shallow-water demosponge faunal connectivity, endemism, and distribution in the Indo-Pacific with a level of resolution unavailable in prior morphology-based studies. LocationDemosponge specimens in this study cover 13 marine provinces of the Indo-Pacific, from the Red Sea to South East Polynesia. MethodsWe classified demosponge barcodes using the ribosomal subunit (28S rDNA) of 1,910 sponge samples into molecular operational taxonomic units (MOTUs). MOTU composition of the 13 marine provinces was compared based on Jaccard and Sorenson dissimilarities, and other biodiversity indices. ResultsOur data corroborated high levels of endemism among demosponges. Faunal overlaps were revealed between the Red Sea and the Gulf, which displayed relatively small connectivity with other marine provinces of the Western Indian Ocean. In the Western Indian Ocean, we observed a strong faunistic boundary to the Central Indo-Pacific. The Polynesian sponge faunas were comparatively isolated marine provinces of the Central Indo-Pacific. Main conclusionsOur data corroborate case studies on sponges that generally reject the presence of cosmopolitan or otherwise widespread sponge species, instead revealing high levels of regional endemism. This is consistent with similar observations and hypotheses in other marine invertebrates. Connectivity among Indo-Pacific marine provinces differs for demosponges in many aspects from that of other marine taxa, such as corals and fishes, probably due to their shorter pelagic larval phase.

zoology↗

High germline mutation rates but not extreme population size outbreaks influence genetic diversity in crown-of-thorns sea stars

Lewontins paradox, the observation that levels of genetic diversity ({pi}) among animals do not scale linearly with variation in census population sizes (Nc), is an evolutionary conundrum, where the most extreme mismatches between {pi} and Nc are found for highly abundant marine invertebrates. Yet, whether new mutations influence {pi} relative to extrinsic processes remains unknown for most taxa. Here, we provide the first direct germline mutation rate () estimate for a marine invertebrate, using high-coverage (60x) whole-genome sequencing of wild-caught Acanthaster cf. solaris crown-of-thorns sea stars (Echinodermata). We also provide empirical estimates of adult Nc in Australias Great Barrier Reef to jointly examine the determinants of {pi}. Based on direct observations of 63 de novo mutations across 14 parent-offspring trios, the A. cf. solaris mean was 9.13 x 10-09 mutations per-site per-generation (95% CI: 6.51 x 10-09 to 1.18 x 10-08). This value exceeds estimates for other invertebrates, showing greater concordance with reported vertebrate germline mutation rates. Lower-than-expected Ne ([~]70,000-180,000) and low Ne/Nc values (0.0047-0.048) indicated significant genetic drift and weak influences of contemporary population outbreaks on long-term {pi}. Our findings of elevated and low Ne in A. cf. solaris may help explain high mutational loads and extreme polymorphism levels observed in some marine invertebrate taxa and are consistent with evolving in response to Ne (drift-barrier hypothesis). This study advances our understanding of the processes controlling levels of natural genetic variation and provides new data valuable for further testing hypotheses about mutation rate evolution across animal phyla.

evolutionary biology↗

Molecular and mineral responses of corals grown under artificial Calcite Sea conditions

The formation of skeletal structures composed of different calcium carbonate polymorphs (aragonite and calcite) appears to be regulated both biologically and environmentally. Among environmental factors influencing aragonite and calcite precipitation, changes in seawater conditions - primarily in the molar ratio of magnesium and calcium during so-called "Calcite" (mMg:mCa below 2) or "Aragonite" seas (mMg:mCa above 2) - have had profound impacts on the distribution and performance of marine calcifiers throughout the Earths history. Nonetheless, the fossil record shows that some species appear to have counteracted such changes and kept their skeleton polymorph unaltered. Here, the aragonitic octocoral Heliopora coerulea and the aragonitic scleractinian Montipora digitata were exposed to Calcite Sea-like mMg:mCa with various levels of changes in magnesium and calcium concentration, and both mineralogical (i.e., CaCO3 polymorph) and gene expression changes were monitored. Both species maintained aragonite deposition at lower mMg:mCa ratios, while concurrent calcite presence was only detected in M. digitata. Despite a strong variability between independent experimental replicates for both species, the expression for a set of putative calcification-related genes, including known components of scleractinian skeleton organic matrix, was found to consistently change at lower mMg:mCa. These results support previously proposed involvements of the skeleton organic matrix in counteracting decreases in seawater mMg:mCa. Although no consistent changes in expression for calcium and magnesium transporters were observed, down-regulation calcium channels in H. coerulea in one experimental replicate and at an mMg:mCa of 2.5 might indicate the possibility of active calcium uptake regulation by the corals under altered mMg:mCa.

paleontology↗

Improved resolution of recalcitrant nodes in the animal phylogeny through the analysis of genome gene content and morphology

An accurate phylogeny of animals is needed to clarify their evolution, ecology, and impact on shaping the biosphere. Although datasets of several hundred thousand amino acids are nowadays routinely used to test phylogenetic hypotheses, key deep nodes in the metazoan tree remain unresolved: the root of animals, the root of Bilateria, and the monophyly of Deuterostomia. Instead of using the standard approach of amino acid datasets, we performed analyses of newly assembled genome gene content and morphological datasets to investigate these recalcitrant nodes in the phylogeny of animals. We explored extensively the choices for assembling the genome gene content dataset and model choices of morphological analyses. Our results are robust to these choices and provide additional insights into the early evolution of animals, they are consistent with sponges as the sister group of all the other animals, the worm-like bilaterian lineage Xenacoelomorpha as the sister group of the other Bilateria, and tentatively support monophyletic Deuterostomia.

evolutionary biology↗

Transcriptomic response of Cinachyrella cf. cavernosa sponges to spatial competition

Spatial competition in the intertidal zones drives the community structure in marine benthic habitats. Organisms inhabiting these areas not only need to withstand fluctuations of temperature, water level, pH, and salinity, but also need to compete for the best available space. Sponges are key members of the intertidal zones, and their life history processes (e.g. growth, reproduction, and regeneration) are affected by competition. Here we used transcriptomics to investigate the effects of interspecific competition between the tetillid sponge Cinachyrella cf. cavernosa, the zoantharid Zoanthus sansibaricus, and the macroalgae Dictyota ciliolata. The analysis of differentially expressed genes showed that Z. sansibaricus was the most stressful competitor to C. cf. cavernosa, which showed an increased rate of cellular respiration under stress of competition. Similarly, an up-regulation of energy metabolism, lipid metabolism, and the heat-shock protein (HSP) 70 was also observed along with an indication of a viral infection and decreased ability to synthesise protein. A down-regulation of purine and pyrimidine metabolism indicated reduction in physiological activities of the competing sponges. Moreover, a putative case of possible kleptocnidism, not previously reported in Cinachyrella cf. cavernosa was also observed. This study opens the door for more detailed investigations of marine organisms competing for spatial resources using transcriptome data.

ecology↗

TransPi - a comprehensive TRanscriptome ANalysiS PIpeline for de novo transcriptome assembly

The use of RNA-Seq data and the generation of de novo transcriptome assemblies have been pivotal for studies in ecology and evolution. This is distinctly true for non-model organisms, where no genome information is available. Nevertheless, studies of differential gene expression, DNA enrichment baits design, and phylogenetics can all be accomplished with the data gathered at the transcriptomic level. Multiple tools are available for transcriptome assembly, however, no single tool can provide the best assembly for all datasets. Therefore, a multi assembler approach, followed by a reduction step, is often sought to generate an improved representation of the assembly. To reduce errors in these complex analyses while at the same time attaining reproducibility and scalability, automated workflows have been essential in the analysis of RNA-Seq data. However, most of these tools are designed for species where genome data is used as reference for the assembly process, limiting their use in non-model organisms. We present TransPi, a comprehensive pipeline for de novo transcriptome assembly, with minimum user input but without losing the ability of a thorough analysis. A combination of different model organisms, k-mer sets, read lengths, and read quantities were used for assessing the tool. Furthermore, a total of 49 non-model organisms, spanning different phyla, were also analyzed. Compared to approaches using single assemblers only, TransPi produces higher BUSCO completeness percentages, and a concurrent significant reduction in duplication rates. TransPi is easy to configure and can be deployed seamlessly using Conda, Docker and Singularity.

bioinformatics↗

Sponges as bioindicators for microparticulate pollutants

Amongst other threats, the worlds oceans are faced with man-made pollution, including an increasing number of microparticulate pollutants. Sponges, aquatic filter-feeding animals, are able to incorporate fine foreign particles, and thus may be a potential bioindicator for microparticulate pollutants. To address this question, 15 coral reef demosponges sampled around Bangka Island (North Sulawesi, Indonesia) were analyzed for the nature of their foreign particle content using traditional histological methods, advanced light microscopy, and Raman spectroscopy. Sampled sponges accumulated and embedded the very fine sediment fraction (< 200 {micro}m), absent in the surrounding sand, in the ectosome (outer epithelia) and spongin fibers (skeletal elements), which was confirmed by two-photon microscopy. A total of 34 different particle types were identified, of which degraded man-made products, i.e., polystyrene, cotton, titanium dioxide and blue-pigmented particles, were incorporated by eight specimens at concentrations between 91 to 612 particle/g dry sponge tissue. As sponges can weigh several hundreds of grams, we conservatively extrapolate that sponges can incorporate on average 10,000 microparticulate pollutants in their tissue. The uptake of particles, however, appears independent of the material, which suggests that the fluctuation in material ratios is due to the spatial variation of surrounding microparticles. Therefore, sponges have a strong potential to biomonitor microparticulate pollutants, such as microplastics and other degraded industrial products.

ecology↗

The genomic basis of animal origins: a chromosomal perspective from the sponge Ephydatia muelleri

The genomes of non-bilaterian metazoans are key to understanding the molecular basis of early animal evolution. However, a full comprehension of how animal-specific traits such as nervous systems arose is hindered by the scarcity and fragmented nature of genomes from key taxa, such as Porifera. Ephydatia muelleri is a freshwater sponge found across the northern hemisphere. Here we present its 326 Mb genome, assembled to high contiguity (N50: 9.88 Mb) with 23 chromosomes on 24 scaffolds. Our analyses reveal a metazoan-typical genome architecture, with highly shared synteny across Metazoa, and suggest that adaptation to the extreme temperatures and conditions found in freshwater often involves gene duplication. The pancontinental distribution and ready laboratory culture of E. muelleri make this a highly practical model system, which with RNAseq, DNA methylation and bacterial amplicon data spanning its development and range allows exploration of genomic changes both within sponges and in early animal evolution.

evolutionary biology↗

Short-term exposure to high-water temperature causes a shift in the microbiome of the common aquarium sponge Lendenfeldia chondrodes

Marine sponges harbor diverse microbiomes that contribute to their energetic and metabolic needs. Although numerous studies on sponge microbial diversity exist, relatively few focused on sponge microbial community changes under different sources of environmental stress. In this study, we assess the impact of elevated seawater temperature on the microbiome of cultured Lendenfeldia chondrodes, a coral reef sponge commonly found in marine aquaria. Lendenfeldia chondrodes exhibits high thermal tolerance showing no evidence of tissue damage or bleaching at 5 {degrees}C above control water temperature (26 {degrees}C). High-throughput sequencing of the bacterial 16S rRNA V4 region revealed a response of the microbiome of L. chondrodes to short-term exposure to elevated seawater temperature. Shifts in abundance and richness of the dominant bacterial phyla found in the microbiome of this species, namely Proteobacteria, Cyanobacteria, Planctomycetes, and Bacteroidetes, characterized this response. The observed resilience of L. chondrodes and the responsiveness of its microbiome to short-term increases in seawater temperature suggest that this holobiont may be capable of acclimating to anthropogenic-driven sublethal environmental stress via a re-accommodation of its associated bacterial community. This sheds a new light on the potential for resilience of some sponges to increasing surface seawater temperatures and associated projected regime shifts in coral reefs.

ecology↗

Profiling cellular diversity in sponges informs animal cell type and nervous system evolution

The evolutionary origin of metazoan cell types such as neurons, muscles, digestive, and immune cells, remains unsolved. Using whole-body single-cell RNA sequencing in a sponge, an animal without nervous system and musculature, we identify 18 distinct cell types comprising four major families. This includes nitric-oxide sensitive contractile cells, digestive cells active in macropinocytosis, and a family of amoeboid-neuroid cells involved in innate immunity. We uncover presynaptic genes in an amoeboid-neuroid cell type, and postsynaptic genes in digestive choanocytes, suggesting asymmetric and targeted communication. Corroborating this, long neurite-like extensions from neuroid cells directly contact and enwrap choanocyte microvillar collars. Our data indicate a link between neuroid and immune functions in sponges, and suggest that a primordial neuro-immune system cleared intruders and controlled ciliary beating for feeding.

developmental biology↗

A 16S rRNA gene sequencing and analysis protocol for the Illumina MiniSeq platform

High-throughput sequencing of the 16S rRNA gene is widely used in microbial ecology, with Illumina platforms being widely used in recent studies. The MiniSeq, Illuminas latest benchtop sequencer, enables more cost-efficient DNA sequencing relative to larger sequencing platforms (e.g. MiSeq). Here we used a modified custom primer sequencing approach to test the fidelity of the MiniSeq for high-throughput sequencing of the V4 hypervariable region of 16S rRNA genes from complex communities in environmental samples. To this end, we designed an additional sequencing primer that enabled application of a dual-index barcoding method on the MiniSeq. A mock community was sequenced alongside the environmental samples as a quality control benchmark. After careful filtering procedures, we were able to recapture a realistic richness of the mock community, and identify meaningful differences in alpha and beta diversity in the environmental samples. These results show that the MiniSeq can produce similar quantities of high quality V4 reads compared to the MiSeq, yet is a cost-effective option for any laboratory interested in performing high-throughput 16S rRNA gene sequencing.\n\nIMPORTANCEWe modified a custom sequencing approach and used a mock community to test the fidelity of high-throughput sequencing on the Illumina MiniSeq platform. Our results show that the MiniSeq can produce similar quantities of high quality V4 reads compared to the MiSeq. In addition, our protocol increases feasibility for small laboratories to perform their own high-throughput sequencing of the 16S rRNA marker gene.

microbiology↗

A taxogenomics approach uncovers a new genus in the phylum Placozoa

The Placozoa [1] is a monotypic phylum of non-bilaterian marine animals. Its only species, Trichoplax adhaerens, was described in 1883 [2], Despite the worldwide distribution of placozoans [3-6], morphological differences are lacking among isolates from different geographic areas and, consequently, no other species in this phylum has been described and accepted for more than 130 years. However, recent single-gene studies on the genetic diversity of this \"species\" have revealed deeply divergent lineages of, as yet, undefined taxonomic ranks [3,5,6], Since single genes are not considered sufficient to define species [7], a whole nuclear genome comparison appears the most appropriate approach to determine relationships between placozoan lineages. Such a \"taxogenomics\" approach can help discover and diagnose potential additional species and, therefore, develop a much-needed, more robust, taxonomic framework for this phylum. To achieve this we sequenced the genome of a placozoan lineage isolated from Hong Kong (lineage H13), which is distantly related to T. adhaerens [6]. The 87 megabase genome assembly contains 12,010 genes. Comparison to the T. adhaerens genome [8] identified an average protein distance of 24.4% in more than 2,700 screened one-to-one orthologs, similar to levels observed between the chordate classes mammals and birds. Genome rearrangements are commonplace and >25% of genes are not collinear (i.e. they are not in the same order in the two genomes). Finally, a multi-gene distance comparison with other non-bilaterian phyla indicate genus level differences to T. adhaerens. These data highlight the large genomic diversity within the Placozoa and justifies the designation of lineage HI3 as a new species, Xxxxxxxxx yyyyyyyyyyyyy1 gen. et spaec. nov., now the second described placozoan species and the first in a new genus. Phylogenomic analyses furthermore supports a robust placement of the Placozoa as sister to a cnidarian-bilaterian clade.

evolutionary biology↗

Transcriptomic Resilience of a Coral Holobiont to Low pH

Ocean acidification is considered as one of the major threats for coral reefs at a global scale. Marine calcifying organisms, including stony corals, are expected to be the most affected by the predicted decrease of the surface water pH at the end of the century. The severity of the impacts on coral reefs remains as matter of controversy. Although previous studies have explored the physiological response of stony corals to changes in pH, the response of the holobiont (i.e. the coral itself plus its symbionts) remains largely unexplored. In the present study, we assessed the changes in overall gene expression of the coral Montipora digitata and its microalgal symbionts after a short (three days) and a longer (42 days) exposure to low pH (7.6). The short-term exposure to low pH caused small differences in the expression level of the host, impacting mostly genes associated with stress response in other scleractinians. Resilience to Acidification of a Coral Holobiont Longer exposure to low pH resulted in no significant changes in gene expression of the coral host. Gene expression in the eukaryotic symbionts remained unaltered at both exposure times. Our findings suggest resilience, in terms of gene expression, of the Montipora digitata holobiont to pH decrease, as well as capability to acclimatize to extended periods of exposure to low pH.

ecology↗