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Woerheide, G.

Publications and source records attributed to Woerheide, G..

13 recordsLinked to original sources

How Robust are Multispecies Coalescent Species Delimitations in Taxonomically Complex Systems? A Genomic Assessment Using Mediterranean Tethya Sponges

Reliable species delimitation underpins biodiversity assessment but remains difficult for organisms with plastic morphology and few diagnostic characters. Multispecies coalescent (MSC) methods can delimit species from genomic data, yet they are rarely tested in taxonomically complex, marine invertebrate groups where they are arguably most needed. We used the three Mediterranean species of the genus Tethya, a rare, well-characterised system within the otherwise taxonomically difficult phylum Porifera--distinguished by multiple independent morphological and ecological characters--to evaluate how robust MSC-based delimitation is in such groups. Analysing 64 single-copy nuclear loci in BEAST2 and BPP, we compared constrained, hypothesis-testing approaches (BFD*, BFdriver, A10) with freer, heuristic ones (SPEEDEMON, A11), and examined their sensitivity to data type, clock model, priors, and the species-collapse threshold. All methods recovered the three recognised Mediterranean species, but the resolution of within-lineage structure was method-dependent. The hypothesis-testing approaches consistently supported six lineages, robustly across data types and model assumptions, whereas the heuristic approaches proved less stable. Configurations without a priori species hypotheses often failed to converge or were computationally intractable, a problem compounded by the relaxed clock. In SPEEDEMON the outcome changed with the collapse threshold. Because our system lacks an independent reference point to calibrate this threshold, any delimitation based on it is poorly constrained. We conclude that constrained, hypothesis-testing delimitation is the most robust and reproducible MSC approach, yielding a quantitative, model-based hypothesis that can be weighed against other lines of evidence to inform taxonomic decisions. By clarifying how these methods behave and how their outcomes should be interpreted, our study offers a practical guide for researchers working on comparably complex systems.

evolutionary biology↗

Ecological Filtering is a Better Predictor of Microbiome Assembly than Coevolution in Marine Sponges

Understanding how microbiomes evolve in concert with their hosts is crucial for understanding the evolutionary dynamics of complex holobionts. Phylosymbiosis describes a pattern in which microbial community relationships parallel host phylogeny. Although often interpreted as evidence for host-microbiome co-diversification, phylosymbiosis can also arise from ecological filtering, a process in which hosts with similar physiology or morphological characteristics select for similar microbial communities independent of host relatedness. Here, we test co-diversification and ecological filtering as alternative explanations for phylosymbiosis in marine sponges (Order Haplosclerida) from the Red Sea. We inferred a robust host phylogeny using 1,153 target-captured genome-wide loci from 144 specimens and characterised their prokaryotic microbiomes via V4 16S rRNA gene amplicon sequencing. Host clade identity explained [~]50% of the microbiome. However, topological analyses revealed high incongruence between host phylogeny and microbial community composition, and phylogenetic distance was only weakly correlated with microbiome dissimilarity. Partial Mantel tests confirmed that geography did not affect this signal. Trait-based analyses comparing high versus low microbial abundance (HMA-LMA) phenotypes, that are linked to sponge filtration physiology, revealed that this classification was a better predictor of microbiome composition than phylogenetic distance. Furthermore, phylogenetically distant clades with convergent HMA characteristics harboured similar microbiome profiles but had unique amplicon sequence variant (ASV) compositions, with between-trait dissimilarity exceeding within-trait dissimilarity. This demonstrates that sponge-microbiome associations are more influenced by ecological filtering than by host-microbe co-diversification, and suggests that sponge holobionts may be better understood as ecological consortia than as coevolved units.

microbiology↗

Genomic changes are varied across congeneric species pairs

Synteny, the shared arrangement of genes on chromosomes between related species, is a marker of shared ancestry, and synteny-breaking events can result in genomic incompatibilities between populations and ultimately lead to speciation events. Despite its pivotal role as a driver of speciation, the role of synteny breaks on speciation is poorly studied due to a lack of chromosome-level genome assemblies for a taxonomically broad sample of organisms. Here, using 22 congeneric animal genome pairs, we find a link between protein identity, microsynteny, and macrosynteny, but no evidence for a universal path of genomic change during divergence. We observed varied trajectories of synteny conservation relative to protein identity in non-model organisms, with many species pairs showing no karyotypic changes and others displaying large genomic rearrangements. This contrasts with previous studies on model organisms and indicates that the genomic changes preceding or resulting from speciation are likely very contextual between clades.

genomics↗

rRNA depletion for holobiont metatranscriptome profiling across demosponges

Despite the extensive knowledge of sponge microbiome diversity, a critical knowledge gap persists concerning the molecular mechanisms that govern host-symbiont interactions. Deciphering these mechanisms is crucial for understanding how sponge holobionts respond to environmental changes and identifying potential disruptions in sponge-microbe associations. A hindrance to progress in characterizing these molecular crosstalk mechanisms is the scarcity of broadly applicable molecular methods for efficiently sequencing meta-transcriptomes across a diverse array of sponge species. To tackle this challenge, we have introduced a hybrid-capture strategy capable of selectively depleting sponge and bacterial rRNA from total RNA extracts obtained from highly divergent demosponges with varying microbiome complexities. Our innovative pan-demosponge rRNA depletion approach streamlines the efficient characterization of metatranscriptomes within diverse demosponge holobionts, concurrently facilitating the quantification of gene expression in both the host and its microbiome. This methodological advancement represents a significant stride in unraveling the molecular intricacies of sponge-microbe interactions, providing a robust platform for future investigations across a broad spectrum of sponge species.

genomics↗

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↗

Resilience to climate change in an octocoral involves the transcriptional decoupling of the calcification and stress response toolkits

Up to one-third of all described marine species inhabit coral reefs, but the future of these hyperdiverse ecosystems is insecure due to local and global threats, such as overfishing, eutrophication, ocean warming, and acidification. Although these impacts are expected to have a net detrimental effect on reefs, it has been shown that some organisms like octocorals may remain unaffected, or benefit from, anthropogenically induced environmental change, and may replace stony corals in future reefs. Despite their potential importance in future shallow-water coastal environments, the molecular mechanisms leading to the resilience to anthropogenic-induced stress observed in octocorals remain unknown. Here, we use manipulative experiments, proteomics, and transcriptomics to show that the molecular toolkit used by Pinnigorgia flava, a common Indo-Pacific gorgonian octocoral, to deposit its calcium-carbonate skeleton is resilient to heat and seawater acidification stress. Sublethal heat stress triggered a stress response in P. flava but did not affect the expression of 27 transcripts encoding Skeletal Organic Matrix (SOM) proteins. Exposure to seawater acidification did not cause a stress response but triggered the downregulation of many transcripts, including an osteonidogen homolog present in the SOM. The observed transcriptional decoupling of the skeletogenic and stress-response toolkits provides insights into the mechanisms of resilience to anthropogenically-driven environmental change observed in octocorals.

ecology↗

Anaerobic metabolism of Foraminifera thriving below the seafloor

Foraminifera are single-celled eukaryotes (protists) of large ecological importance, as well as environmental and paleoenvironmental indicators and biostratigraphic tools. In addition, they are capable of surviving in anoxic marine environments where they represent a major component of the benthic community. However, the cellular adaptations of Foraminifera to the anoxic environment remain poorly constrained. We sampled an oxic-anoxic transition zone in marine sediments from the Namibian shelf, where the genera Bolivina and Stainforthia dominated the Foraminifera community, and use metatranscriptomics to characterize Foraminifera metabolism across the different geochemical conditions. The relative abundance of Foraminifera gene expression in anoxic sediment depths increased an order of magnitude, which was confirmed in a ten-day incubation experiment where the development of anoxia coincided with a 27-fold increase in the relative abundance of Foraminifera protein encoding transcripts. This indicates that many Foraminifera were not only surviving, but thriving under the anoxic conditions. The anaerobic energy metabolism of these active Foraminifera was characterized by fermentation of sugars and amino acids, dissimilatory nitrate reduction, fumarate reduction, and dephosphorylation of creatine phosphate. This was co-expressed alongside genes involved in production of reticulopodia, phagocytosis, calcification, and clathrin-mediated-endocytosis (CME). Thus, Foraminifera may use CME under anoxic conditions to utilize dissolved organic matter as a carbon and energy source, in addition to ingestion of prey cells via phagocytosis. These mechanisms help explain how some Foraminifera can thrive under anoxia, which would help to explain their ecological success documented in the fossil record since the Cambrian period more than 500 million years ago.

microbiology↗

Textile waste and microplastic induce activity and development of unique hydrocarbon-degrading marine bacterial communities

Biofilm-forming microbial communities on plastics and textile fibers are of growing interest since they have potential to contribute to disease outbreaks and material biodegradability in the environment. Knowledge on microbial colonization of pollutants in the marine realm is expanding, but metabolic responses during substrate colonization remains poorly understood. Here, we assess the metabolic response in marine microbial communities to three different micropollutants, virgin high-density polyethylene (HDPE) microbeads, polysorbate-20 (Tween), and textile fibers. Intertidal textile fibers, mainly cotton, virgin HDPE, and Tween induced variable levels of microbial growth, respiration, and community assembly in controlled microcosm experiments. RAMAN characterization of the chemical composition of the textile waste fibers and high-throughput DNA sequencing data shows how the increased metabolic stimulation and biodegradation is translated into selection processes ultimately manifested in different communities colonizing the different micropollutant substrates. The composition of the bacterial communities colonizing the substrates were significantly altered by micropollutant substrate type and light conditions. Bacterial taxa, closely related to the well-known hydrocarbonoclastic bacteria Kordiimonas spp. and Alcanivorax spp., were enriched in the presence of textile-waste. The findings demonstrate an increased metabolic response by marine hydrocarbon-degrading bacterial taxa in the presence of microplastics and textile waste, highlighting their biodegradation potential. The metabolic stimulation by the micropollutants was increased in the presence of light, possibly due to photochemical dissolution of the plastic into smaller bioavailable compounds. Our results suggest that the development and increased activity of these unique microbial communities likely play a role in the bioremediation of the relatively long lived textile and microplastic pollutants in marine habitats. Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=104 SRC="FIGDIR/small/939876v1_ufig1.gif" ALT="Figure 1"> View larger version (40K): org.highwire.dtl.DTLVardef@19322f3org.highwire.dtl.DTLVardef@dbae7dorg.highwire.dtl.DTLVardef@9c9d4aorg.highwire.dtl.DTLVardef@1aa636_HPS_FORMAT_FIGEXP M_FIG C_FIG

microbiology↗

Comparative proteomics of octocoral and scleractinian skeletomes and the evolution of coral calcification

Corals are ecosystem engineers of the coral reefs, one of the most biodiverse but severely threatened marine ecosystems. The ability of corals to form the three dimensional structure of reefs depends on the precipitation of calcium carbonate under biologically control. However, the exact mechanisms underlying this biologically controlled biomineralization remain to be fully unelucidated, for example whether corals employ a different molecular machinery for the deposition of different calcium carbonate (CaCO3) polymorphs (i.e., aragonite or calcite). Here we used tandem mass spectrometry (MS/MS) to compare skeletogenic proteins, i.e., the proteins occluded in the skeleton of three octocoral and one scleractinian species: Tubipora musica and Sinularia cf. cruciata, both forming calcite sclerites, the blue coral Heliopora coerulea with an aragonitic rigid skeleton, and the scleractinian aragonitic Montipora digitata. We observed extremely low overlap between aragonitic and calcitic species, while a core set of proteins is shared between octocorals producing calcite sclerites. However, the same carbonic anhydrase (CruCA4) is employed for the formation of skeletons of both polymorphs. Similarities could also be observed between octocorals and scleractinians, including the presence of a galaxin-like protein. Additionally, as in scleractinians, some octocoral skeletogenic proteins, such as acidic proteins and scleritin, appear to have been secondarily co-opted for calcification and likely derive from proteins playing different extracellular functions. In H. coerulea, co-option was characterized by aspartic acid-enrichment of proteins. This work represents the first attempt to identify the molecular basis underlying coral skeleton polymorph diversity, providing several new research targets and enabling both future functional and evolutionary studies aimed at elucidating the origin and evolution of biomineralization in corals.

evolutionary biology↗

New non-bilaterian transcriptomes provide novel insights into the evolution of coral skeletomes

A general feature of animal skeletomes is the co-presence of taxonomically widespread and lineage-specific proteins that actively regulate the biomineralization process. Among cnidarians, the skeletomes of scleractinian corals have been shown to follow this trend, however in this group distribution and phylogenetic analyses of biomineralization-related genes have been often based on limited numbers of species, with other anthozoan calcifiers such as octocorals, being overlooked. We de-novo sequenced the transcriptomes of four soft-coral species characterized by different calcification strategies (aragonite skeleton vs. calcitic sclerites) and data-mined published non-bilaterian transcriptomic resources to construct a taxonomically comprehensive sequence database to map the distribution of scleractinian and octocoral skeletome components. At the large scale, no protein showed a Cnidaria+Placozoa or Cnidaria+Ctenophora distribution, while some were found in cnidarians and Porifera. Within Scleractinia and Octocorallia, we expanded the distribution for several taxonomically restricted genes (TRGs) and propose an alternative evolutionary scenario, involving an early single biomineralization-recruitment event, for galaxin sensu stricto. Additionally, we show that the enrichment of acidic residues within skeletogenic proteins did not occur at the Corallimorpharia-Scleractinia transition, but appears to be associated with protein secretion in the organic matrix. Finally, the distribution of octocoral calcification-related proteins appears independent of skeleton mineralogy (i.e. aragonite/calcite) with no differences on the proportion of shared skeletogenic proteins between scleractinians and aragonitic or calcitic octocorals. This points to skeletome homogeneity within but not between groups of calcifying cnidarians, although some proteins like galaxins and SCRiP-3a could represent instances of commonality.

evolutionary 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↗

Divergence times in demosponges (Porifera): firstinsights from new mitogenomes and the inclusion offossils in a birth-death clock model

Approximately 80% of all recent sponge species belong to the class Demospongiae. Yet, despite their diversity and importance, accurate divergence times are still unknown for most demosponge clades. The estimation of demosponge divergence time is key to answering fundamental questions like e.g. the origin of Demospongiae, their diversification and historical biogeography. Molecular sequence data alone is not informative on an absolute time scale, and therefore needs to be \"calibrated\" with additional data such as fossils. Here, we apply the fossilized birth-death model (FBD), which has the advantage, compared to strict node dating with the oldest fossil occurrences, that it allows for the inclusion of young and old fossils in the analysis of divergence time. We use desma-bearing sponges, a diverse group of demosponges that form rigid skeletons and have a rich and continuous fossil record dating back to the Cambrian ([~]500 Ma), aiming to date the demosponge radiation and constrain the timing of key evolutionary events, like the transition from marine to freshwater habitats. To do so, we assembled mitochondrial genomes of six desma-bearing demosponges from size-selected reduced-representation genomic libraries and apply a fossilized birth-death model including 30 fossils and 33 complete demosponge mitochondrial genomes to infer a dated phylogeny of Demospongiae. Our study supports a Neoproterozoic origin of Demospongiae. Novel age estimates for the split of freshwater and marine sponges dating back to the Carboniferous and the previously assumed Recent ([~]18 Ma) diversification of freshwater sponges is supported. Moreover, we provide detailed age estimates for a possible diversification of Tetractinellidae ([~]315 Ma), the Astrophorina ([~]240 Ma), the Spirophorina ([~]120 Ma) and the family Corallistidae ([~]188 Ma) all of which are considered as key groups for dating the Demospongiae, due to their extraordinary rich and continuous fossil history.

evolutionary biology↗

Mitochondrial RNA processing in absence of tRNApunctuations in octocorals

BackgroundMitogenome diversity is staggering among early branching animals with respect to size, gene density and content, gene orders, and number of tRNA genes, especially in cnidarians. This last point is of special interest as tRNA cleavage drives the maturation of mitochondrial mRNAs and is a primary mechanism for mt-RNA processing in animals. Mitochondrial RNA processing in non-bilaterian metazoans, some of which possess a single tRNA gene in their mitogenomes, is essentially unstudied despite its importance in understanding the evolution of mitochondrial transcription in animals.\n\nResultsWe characterized the mature mitochondrial mRNA transcripts in a species of the octocoral genus Sinularia (Alcyoniidae: Octocorallia), and defined precise boundaries of transcription units using different molecular methods. Most mt-mRNAs were polycistronic units containing two or three genes and 5 and/or 3 untranslated regions (UTRs) of varied length. The octocoral specific, mtDNA-encoded mismatch repair gene, mtMutS, was found to undergo alternative polyadenylation (APA), and exhibited differential expression of alternate transcripts suggesting a unique regulatory mechanism for this gene. In addition, a long noncoding RNA complementary to the ATP6 gene (lncATP6) potentially involved in antisense regulation was detected.\n\nConclusionsMt-mRNA processing in octocorals bearing a single mt-tRNA is complex. Considering the variety of mitogenome arrangements known in cnidarians, and in general among non-bilaterian metazoans, our findings provide a first glimpse into the complex mtDNA transcription, mt-mRNA processing, and regulation among early branching animals and represents a first step towards understanding its functional and evolutionary implications.

molecular biology↗