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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. Reconstructing the early molecular evolution of animals requires genomic resources for non-bilaterian animals. Here, the authors present the chromosome-level genome of a freshwater sponge together with analyses of its genome architecture, methylation, developmental gene expression, and microbiome.

The phylogenetic placement of the morphologically simple placozoans is crucial to understanding the evolution of complex animal traits. Here, we examine the influence of adding new genomes from placozoans to a large dataset designed to study the deepest splits in the animal phylogeny. Using site-heterogeneous substitution models, we show that it is possible to obtain strong support, in both amino acid and reduced-alphabet matrices, for either a sister-group relationship between Cnidaria and Placozoa, or for Cnidaria and Bilateria as seen in most published work to date, depending on the orthologues selected to construct the matrix. We demonstrate that a majority of genes show evidence of compositional heterogeneity, and that support for the Cnidaria + Bilateria clade can be assigned to this source of systematic error. In interpreting these results, we caution against a peremptory reading of placozoans as secondarily reduced forms of little relevance to broader discussions of early animal evolution. Filter-feeding sponges and tiny gliding, pancake-like animals called placozoans are the only two major groups of animals that lack muscles, nerves and an internal gut. Sponges have historically been seen as the first to have branched off in animal phylogeny – the family tree of living organisms that shows how species are related. This is because it is assumed that they split from the other animals before features including muscles, nerves and internal guts evolved. Sequences of their genetic material (the genome) support this view, although some argue that jellyfish-like animals called ctenophores branched first. One explanation for this disagreement is that ctenophores use different proportions of amino acids in their proteins, known as compositional heterogeneity. Computer algorithms that assume amino acid usage is the same universally throughout evolution may therefore place ctenophores incorrectly. In contrast, so far the only genome from a placozoan shows that they are equally closely related to jellyfish and corals (cnidarians) and bilaterians, which includes worms, insects and vertebrates. To test whether this view of the first branches of the animal tree of life is correct, Laumer et al. included the genomes from several undescribed species of placozoans in a phylogenetic analysis. These analyses showed a relationship that had not previously been seen. The placozoans were the closest living relative to cnidarians. However, when looking at the level of genes rather than whole genomes, the more usual relationship of placozoans being equally related to cnidarians and bilaterians re-emerged. To resolve this conflict, Laumer et al. focused on the genes that had the least compositional heterogeneity. When doing this, the relationship appeared to be the newly identified one of placozoans being most closely related to cnidarians. Researchers studying cnidarians often hope to find some clues as to how the complex features they seem to share with bilaterians originated. The findings of Laumer et al. may suggest that the ancestors of the placozoans did in fact have muscles, nerves and guts, but they lost these traits in favor of a simpler lifestyle. An alternative, but controversial possibility is that the ancestor of cnidarians and bilaterians was a simple organism like a placozoan, and the two evolved their complex traits independently. The findings show a complex picture of early animal evolution. Further study of placozoans may well clarify this picture.

In the deep ocean symbioses between microbes and invertebrates are emerging as key drivers of ecosystem health and services. We present a large-scale analysis of microbial diversity in deep-sea sponges (Porifera) from scales of sponge individuals to ocean basins, covering 52 locations, 1077 host individuals translating into 169 sponge species (including understudied glass sponges), and 469 reference samples, collected anew during 21 ship-based expeditions. We demonstrate the impacts of the sponge microbial abundance status, geographic distance, sponge phylogeny, and the physical-biogeochemical environment as drivers of microbiome composition, in descending order of relevance. Our study further discloses that fundamental concepts of sponge microbiology apply robustly to sponges from the deep-sea across distances of >10,000 km. Deep-sea sponge microbiomes are less complex, yet more heterogeneous, than their shallow-water counterparts. Our analysis underscores the uniqueness of each deep-sea sponge ground based on which we provide critical knowledge for conservation of these vulnerable ecosystems. This study presents a large-scale analysis of microbial diversity in deep-sea sponges. They show that sponge microbial abundance status, geographic distance, sponge phylogeny and the physical-biogeochemical environment drive microbiome composition, in descending order of relevance. The uniqueness of each deep-sea sponge ground stresses the need for their strategic preservation.

Sponges contain an astounding diversity of lipids that serve in several biological functions, including yolk formation in their oocytes and embryos. The study of lipid metabolism during reproduction can provide information on food-web dynamics and energetic needs of the populations in their habitats, however, there are no studies focusing on the lipid metabolism of sponges during their seasonal reproduction. In this study, we used histology, lipidome profiling (UHPLC-MS), and transcriptomic analysis (RNA-seq) on the deep-sea sponge Phakellia ventilabrum (Demospongiae, Bubarida), a key species of North-Atlantic sponge grounds, with the goal to (i) assess the reproductive strategy and seasonality of this species, (ii) examine the relative changes in the lipidome signal and the gene expression patterns of the enzymes participating in lipid metabolism during oogenesis. Phakellia ventilabrum is an oviparous and most certainly gonochoristic species, reproducing in May and September in the different studied areas. Half of the specimens were reproducing, generating two to five oocytes per mm 2 . Oocytes accumulated lipid droplets and as oogenesis progressed, the signal of most of the unsaturated and monounsaturated triacylglycerides increased, as well as of a few other phospholipids. In parallel, we detected upregulation of genes in female tissues related to triacylglyceride biosynthesis and others related to fatty acid beta-oxidation. Triacylglycerides are likely the main type of lipid forming the yolk in P. ventilabrum since this lipid category has the most marked changes. In parallel, other lipid categories were engaged in fatty acid beta-oxidation to cover the energy requirements of female individuals during oogenesis. In this study, the reproductive activity of the sponge P. ventilabrum was studied for the first time uncovering their seasonality and revealing 759 lipids, including 155 triacylglycerides. Our study has ecological and evolutionary implications providing essential information for understanding the molecular basis of reproduction and the origins and formation of lipid yolk in early-branching metazoans.

Sponges (Porifera) are among the earliest evolving metazoans. Their filter-feeding body plan based on choanocyte chambers organized into a complex aquiferous system is so unique among metazoans that it either reflects an early divergence from other animals prior to the evolution of features such as muscles and nerves, or that sponges lost these characters. Analyses of the Amphimedon and Oscarella genomes support this view of uniqueness—many key metazoan genes are absent in these sponges—but whether this is generally true of other sponges remains unknown. We studied the transcriptomes of eight sponge species in four classes (Hexactinellida, Demospongiae, Homoscleromorpha, and Calcarea) specifically seeking genes and pathways considered to be involved in animal complexity. For reference, we also sought these genes in transcriptomes and genomes of three unicellular opisthokonts, two sponges (A. queenslandica and O. carmela), and two bilaterian taxa. Our analyses showed that all sponge classes share an unexpectedly large complement of genes with other metazoans. Interestingly, hexactinellid, calcareous, and homoscleromorph sponges share more genes with bilaterians than with nonbilaterian metazoans. We were surprised to find representatives of most molecules involved in cell–cell communication, signaling, complex epithelia, immune recognition, and germ-lineage/sex, with only a few, but potentially key, absences. A noteworthy finding was that some important genes were absent from all demosponges (transcriptomes and the Amphimedon genome), which might reflect divergence from main-stem lineages including hexactinellids, calcareous sponges, and homoscleromorphs. Our results suggest that genetic complexity arose early in evolution as shown by the presence of these genes in most of the animal lineages, which suggests sponges either possess cryptic physiological and morphological complexity and/or have lost ancestral cell types or physiological processes.

Sponges are a dominant element of the Antarctic benthic communities, posing both high species richness and large population densities. Despite their importance in Antarctic ecosystems, very little is known about their reproductive patterns and strategies. In our study, we surveyed the tissue of six different species for reproductive elements, namely, Dendrilla antarctica Topsent, 1905 (order Dendroceratida), Phorbas areolatus (Thiele, 1905), Kirkpatrickia variolosa (Kirkpatrick, 1907), and Isodictya kerguelenensis (Ridley & Dendy, 1886) (order Poecilosclerida), and Hemigellius pilosus (Kirkpatrick, 1907) and Haliclona penicillata (Topsent, 1908) (Haplosclerida). Samples of these six species containing various reproductive elements were collected in Deception Island and were processed for both light and transmission electron microscopy (TEM). Even though we were not able to monitor the entire reproductive cycle, due to time and meteorological conditions, we report important aspects of the reproduction of these species. This includes oocyte and embryo morphology and cell ultrastructure, follicular structures and nurse cell activity, as well as vitellogenesis. All species were brooding their embryos within their mesohyl. Both oocytes and embryos were registered in the majority of the studied species, and a single sperm cell being carried to an egg for fertilization was observed in H. penicillata. While the reproductive periods of all species coincided temporally, some of them seemed to rely on a single spawning event, this being suggested by the synchronic oogenesis and embryogenesis occurrence of D. antarctica, P. areolatus and I. kerguelenensis. In contrast, K. variolosa had an asynchronous embryo development, which suggests several larval release events. Our results suggest that differences in the reproductive strategies and morphological traits might succeed in the coexistence of these species at the same habitat avoiding the direct competition between them.

Sponges are interesting animal models for regeneration studies, since even from dissociated cells, they are able to regenerate completely. In particular, explants are model systems that can be applied to many sponge species, since small fragments of sponges can regenerate all elements of the adult, including the oscula and the ability to pump water. The morphological aspects of regeneration in sponges are relatively well known, but the molecular machinery is only now starting to be elucidated for some sponge species. Here, we have used an explant system of the demosponge Halichondria panicea to understand the molecular machinery deployed during regeneration of the aquiferous system. We sequenced the transcriptomes of four replicates of the 5–day explant without an osculum (NOE), four replicates of the 17–18–day explant with a single osculum and pumping activity (PE) and also four replicates of field–collected individuals with regular pumping activity (PA), and performed differential gene expression analysis. We also described the morphology of NOE and PE samples using light and electron microscopy. Our results showed a highly disorganised mesohyl and disarranged aquiferous system in NOE that is coupled with upregulated pathways of ciliogenesis, organisation of the ECM, and cell proliferation and survival. Once the osculum is formed, genes involved in “response to stimulus in other organisms” were upregulated. Interestingly, the main molecular machinery of vasculogenesis described in vertebrates was activated during the regeneration of the aquiferous system. Notably, vasculogenesis markers were upregulated when the tissue was disorganised and about to start forming canals (NOE) and angiogenic stimulators and ECM remodelling machineries were differentially expressed once the aquiferous system was in place (PE and PA). Our results are fundamental to better understanding the molecular mechanisms involved in the formation of the aquiferous system in sponges, and its similarities with the early onset of blood-vessel formation in animal evolution.

Background Sponge holobionts (i.e., the host and its associated microbiota) play a key role in the cycling of dissolved organic matter (DOM) in marine ecosystems. On coral reefs, an ecological shift from coral-dominated to algal-dominated ecosystems is currently occurring. Given that benthic corals and macroalgae release different types of DOM, in different abundances and with different bioavailability to sponge holobionts, it is important to understand how the metabolic activity of the host and associated microbiota change in response to the exposure to both DOM sources. Here, we look at the differential gene expression of two sponge holobionts 6 hours after feeding on naturally sourced coral- and macroalgal-DOM using RNA sequencing and meta-transcriptomic analysis. Results We found a slight, but significant differential gene expression in the comparison between the coral- and macroalgal-DOM treatments in both the high microbial abundance sponge Plakortis angulospiculatus and the low microbial abundance sponge Haliclona vansoesti . In the hosts, processes that regulate immune response, signal transduction, and metabolic pathways related to cell proliferation were elicited. In the associated microbiota carbohydrate metabolism was upregulated in both treatments, but coral-DOM induced further lipid and amino acids biosynthesis, while macroalgal-DOM caused a stress response. These differences could be driven by the presence of distinct organic macronutrients in the two DOM sources and of small pathogens or bacterial virulence factors in the macroalgal-DOM. Conclusions This work provides two new sponge meta-transcriptomes and a database of putative genes and genetic pathways that are involved in the differential processing of coral- versus macroalgal-DOM as food source to sponges with high and low abundances of associated microbes. These pathways include carbohydrate metabolism, signaling pathways, and immune responses. However, the differences in the meta-transcriptomic responses of the sponge holobionts after 6 hours of feeding on the two DOM sources were small. Longer-term responses to both DOM sources should be assessed to evaluate how the metabolism and the ecological function of sponges will be affected when reefs shift from coral towards algal dominance.

Sponges are key ecosystem engineers that shape, structure and enhance the biodiversity of marine benthic communities globally. Sponge aggregations and reefs are recognized as vulnerable marine ecosystems (or VMEs) due to their susceptibility to damage from bottom-contact fishing gears. Ensuring their long-term sustainability, preservation, and ecosystem functions requires the implementation of sound scientific conservation tools. Here, the genetic diversity, structure, and connectivity of the deep-sea glass sponge, Vazella pourtalesii (Schmidt, 1870), was investigated using 1,102 neutral SNPs obtained in RADseq. This species is distributed across the northwest Atlantic from Florida, USA to Nova Scotia, Canada and we sequenced samples covering this full distribution and provided evidence of strong genetic structure with two distinct clusters: Florida together with the Carolina Shelves and the Scotian Shelf. We estimated moderate levels of diversity with low migration across large distances (> 1000 kms) and high connectivity at smaller scales (< 300 kms). Further, fishing pressure on genetic diversity was evaluated, within two Sponge Conservation Areas (SCAs) on the Scotian Shelf. Those areas have different disturbance histories, and cumulative fishing pressure. Slightly lower levels of genetic diversity were found inside the SCAs, and yet they encompassed a high proportion of the diversity observed within the Scotian Shelf. We provide baseline data for future monitoring of the SCAs, discussing our findings in the light of existing area-based management tools.

Background One of the hallmarks of multicellular organisms is the ability of their cells to trigger responses to the environment in a coordinated manner. In recent years primary cilia have been shown to be present as ‘antennae’ on almost all animal cells, and are involved in cell-to-cell signaling in development and tissue homeostasis; how this sophisticated sensory system arose has been little-studied and its evolution is key to understanding how sensation arose in the Animal Kingdom. Sponges (Porifera), one of the earliest evolving phyla, lack conventional muscles and nerves and yet sense and respond to changes in their fluid environment. Here we demonstrate the presence of non-motile cilia in sponges and studied their role as flow sensors. Results Demosponges excrete wastes from their body with a stereotypic series of whole-body contractions using a structure called the osculum to regulate the water-flow through the body. In this study we show that short cilia line the inner epithelium of the sponge osculum. Ultrastructure of the cilia shows an absence of a central pair of microtubules and high speed imaging shows they are non-motile, suggesting they are not involved in generating flow. In other animals non-motile, ‘primary’, cilia are involved in sensation. Here we show that molecules known to block cationic ion channels in primary cilia and which inhibit sensory function in other organisms reduce or eliminate sponge contractions. Removal of the cilia using chloral hydrate, or removal of the whole osculum, also stops the contractions; in all instances the effect is reversible, suggesting that the cilia are involved in sensation. An analysis of sponge transcriptomes shows the presence of several transient receptor potential (TRP) channels including PKD channels known to be involved in sensing changes in flow in other animals. Together these data suggest that cilia in sponge oscula are involved in flow sensation and coordination of simple behaviour. Conclusions This is the first evidence of arrays of non-motile cilia in sponge oscula. Our findings provide support for the hypothesis that the cilia are sensory, and if true, the osculum may be considered a sensory organ that is used to coordinate whole animal responses in sponges. Arrays of primary cilia like these could represent the first step in the evolution of sensory and coordination systems in metazoans.