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PIWI proteins use PIWI-interacting RNAs (piRNAs) to identify and silence transposable elements and thereby maintain genome integrity between metazoan generations 1 . The targeting of transposable elements by PIWI has been compared to mRNA target recognition by Argonaute proteins 2 , 3 , which use microRNA (miRNA) guides, but the extent to which piRNAs resemble miRNAs is not known. Here we present cryo-electron microscopy structures of a PIWI–piRNA complex from the sponge Ephydatia fluviatilis with and without target RNAs, and a biochemical analysis of target recognition. Mirroring Argonaute, PIWI identifies targets using the piRNA seed region. However, PIWI creates a much weaker seed so that stable target association requires further piRNA–target pairing, making piRNAs less promiscuous than miRNAs. Beyond the seed, the structure of PIWI facilitates piRNA–target pairing in a manner that is tolerant of mismatches, leading to long-lived PIWI–piRNA–target interactions that may accumulate on transposable-element transcripts. PIWI ensures targeting fidelity by physically blocking the propagation of piRNA–target interactions in the absence of faithful seed pairing, and by requiring an extended piRNA–target duplex to reach an endonucleolytically active conformation. PIWI proteins thereby minimize off-targeting cellular mRNAs while defending against evolving genomic threats. Cryo-electron microscopy structures of a PIWI–piRNA complex provide insight into how piRNAs recognise target RNAs and reveal differences from the target mechanisms of microRNAs.

Molecular fossils (or biomarkers) are key to unraveling the deep history of eukaryotes, especially in the absence of traditional fossils. In this regard, the sterane 24-isopropylcholestane has been proposed as a molecular fossil for sponges, and could represent the oldest evidence for animal life. The sterane is found in rocks ∼650–540 million y old, and its sterol precursor (24-isopropylcholesterol, or 24-ipc) is synthesized today by certain sea sponges. However, 24-ipc is also produced in trace amounts by distantly related pelagophyte algae, whereas only a few close relatives of sponges have been assayed for sterols. In this study, we analyzed the sterol and gene repertoires of four taxa (Salpingoeca rosetta, Capsaspora owczarzaki, Sphaeroforma arctica, and Creolimax fragrantissima), which collectively represent the major living animal outgroups. We discovered that all four taxa lack C30 sterols, including 24-ipc. By building phylogenetic trees for key enzymes in 24-ipc biosynthesis, we identified a candidate gene (carbon-24/28 sterol methyltransferase, or SMT) responsible for 24-ipc production. Our results suggest that pelagophytes and sponges independently evolved C30 sterol biosynthesis through clade-specific SMT duplications. Using a molecular clock approach, we demonstrate that the relevant sponge SMT duplication event overlapped with the appearance of 24-isopropylcholestanes in the Neoproterozoic, but that the algal SMT duplication event occurred later in the Phanerozoic. Subsequently, pelagophyte algae and their relatives are an unlikely alternative to sponges as a source of Neoproterozoic 24-isopropylcholestanes, consistent with growing evidence that sponges evolved long before the Cambrian explosion ∼542 million y ago.

The recognition that all macroorganisms live in symbiotic association with microbial communities has opened up a new field in biology. Animals, plants, and algae are now considered holobionts, complex ecosystems consisting of the host, the microbiota, and the interactions among them. Accordingly, ecological concepts can be applied to understand the host-derived and microbial processes that govern the dynamics of the interactive networks within the holobiont. In marine systems, holobionts are further integrated into larger and more complex communities and ecosystems, a concept referred to as “nested ecosystems.” In this review, we discuss the concept of holobionts as dynamic ecosystems that interact at multiple scales and respond to environmental change. We focus on the symbiosis of sponges with their microbial communities—a symbiosis that has resulted in one of the most diverse and complex holobionts in the marine environment. In recent years, the field of sponge microbiology has remarkably advanced in terms of curated databases, standardized protocols, and information on the functions of the microbiota. Like a Russian doll, these microbial processes are translated into sponge holobiont functions that impact the surrounding ecosystem. For example, the sponge-associated microbial metabolisms, fueled by the high filtering capacity of the sponge host, substantially affect the biogeochemical cycling of key nutrients like carbon, nitrogen, and phosphorous. Since sponge holobionts are increasingly threatened by anthropogenic stressors that jeopardize the stability of the holobiont ecosystem, we discuss the link between environmental perturbations, dysbiosis, and sponge diseases. Experimental studies suggest that the microbial community composition is tightly linked to holobiont health, but whether dysbiosis is a cause or a consequence of holobiont collapse remains unresolved. Moreover, the potential role of the microbiome in mediating the capacity for holobionts to acclimate and adapt to environmental change is unknown. Future studies should aim to identify the mechanisms underlying holobiont dynamics at multiple scales, from the microbiome to the ecosystem, and develop management strategies to preserve the key functions provided by the sponge holobiont in our present and future oceans.

Cultivated bacteria such as actinomycetes are a highly useful source of biomedically important natural products. However, such ‘talented’ producers represent only a minute fraction of the entire, mostly uncultivated, prokaryotic diversity. The uncultured majority is generally perceived as a large, untapped resource of new drug candidates, but so far it is unknown whether taxa containing talented bacteria indeed exist. Here we report the single-cell- and metagenomics-based discovery of such producers. Two phylotypes of the candidate genus ‘ Entotheonella ’ with genomes of greater than 9 megabases and multiple, distinct biosynthetic gene clusters co-inhabit the chemically and microbially rich marine sponge Theonella swinhoei . Almost all bioactive polyketides and peptides known from this animal were attributed to a single phylotype. ‘ Entotheonella ’ spp. are widely distributed in sponges and belong to an environmental taxon proposed here as candidate phylum ‘Tectomicrobia’. The pronounced bioactivities and chemical uniqueness of ‘ Entotheonella ’ compounds provide significant opportunities for ecological studies and drug discovery. Single-cell- and metagenomics-based study reveals two members of the candidate genus ‘ Entotheonella ’, symbionts of the marine sponge Theonella swinhoei ; distinct biosynthetic gene clusters that account for most of the bioactive polyketides and peptides known from T. swinhoei are shown to be attributable to a single member of the T. swinhoei Y microbiome. Chemical diversity in marine microbes Almost all drugs and drug candidates from bacteria are produced by a few groups of metabolically rich organisms. That leaves the unculturable — or uncultivated — microbial majority as a largely untapped resource. Here Jörn Piel and colleagues report the use of single-cell and metagenomic analysis to identify two potential 'environmental factories', both members of the candidate genus Entotheonella and symbionts of the chemically rich marine sponge Theonella swinhoei . Importantly they find that the genomes of both microbes encode multiple distinct biosynthetic gene clusters that together account for most of the bioactive polyketides and peptides previously thought to be produced by the sponge host. This discovery identifies Entotheonella and members of the newly proposed phylum Tectomicrobia as a 'biochemically talented' phylum on a par with the actinomycetes.

The marine environment is home to a taxonomically diverse ecosystem. Organisms such as algae, molluscs, sponges, corals, and tunicates have evolved to survive the high concentrations of infectious and surface-fouling bacteria that are indigenous to ocean waters. Both macroalgae (seaweeds) and microalgae (diatoms) contain pharmacologically active compounds such as phlorotannins, fatty acids, polysaccharides, peptides, and terpenes which combat bacterial invasion. The resistance of pathogenic bacteria to existing antibiotics has become a global epidemic. Marine algae derivatives have shown promise as candidates in novel, antibacterial drug discovery. The efficacy of these compounds, their mechanism of action, applications as antibiotics, disinfectants, and inhibitors of foodborne pathogenic and spoilage bacteria are reviewed in this article.

The as-yet uncultured filamentous bacteria “Candidatus Entotheonella factor” and “Candidatus Entotheonella gemina” live associated with the marine sponge Theonella swinhoei Y, the source of numerous unusual bioactive natural products. Belonging to the proposed candidate phylum “Tectomicrobia,” Candidatus Entotheonella members are only distantly related to any cultivated organism. The Ca. E. factor has been identified as the source of almost all polyketide and modified peptides families reported from the sponge host, and both Ca. Entotheonella phylotypes contain numerous additional genes for as-yet unknown metabolites. Here, we provide insights into the biology of these remarkable bacteria using genomic, (meta)proteomic, and chemical methods. The data suggest a metabolic model of Ca. Entotheonella as facultative anaerobic, organotrophic organisms with the ability to use methanol as an energy source. The symbionts appear to be auxotrophic for some vitamins, but have the potential to produce most amino acids as well as rare cofactors like coenzyme F420. The latter likely accounts for the strong autofluorescence of Ca. Entotheonella filaments. A large expansion of protein families involved in regulation and conversion of organic molecules indicates roles in host–bacterial interaction. In addition, a massive overrepresentation of members of the luciferase-like monooxygenase superfamily points toward an important role of these proteins in Ca. Entotheonella. Furthermore, we performed mass spectrometric imaging combined with fluorescence in situ hybridization to localize Ca. Entotheonella and some of the bioactive natural products in the sponge tissue. These metabolic insights into a new candidate phylum offer hints on the targeted cultivation of the chemically most prolific microorganisms known from microbial dark matter.

Relatively little is known about the role of sponge microbiomes in the Antarctic marine environment, where sponges may dominate the benthic landscape. Specifically, we understand little about how taxonomic and functional diversity contributes to the symbiotic lifestyle and aids in nutrient cycling. Here we use functional metagenomics to investigate the community composition and metabolic potential of microbiomes from two abundant Antarctic sponges, Leucetta antarctica and Myxilla sp. Genomic and taxonomic analyses show that both sponges harbor a distinct microbial community with high fungal abundance, which differs from the surrounding seawater. Functional analyses reveal both sponge-associated microbial communities are enriched in functions related to the symbiotic lifestyle (e.g., CRISPR system, Eukaryotic-like proteins, and transposases), and in functions important for nutrient cycling. Both sponge microbiomes possessed genes necessary to perform processes important to nitrogen cycling (i.e., ammonia oxidation, nitrite oxidation, and denitrification), and carbon fixation. The latter indicates that Antarctic sponge microorganisms prefer light-independent pathways for CO 2 fixation mediated by chemoautotrophic microorganisms. Together, these results show how the unique metabolic potential of two Antarctic sponge microbiomes help these sponge holobionts survive in these inhospitable environments, and contribute to major nutrient cycles of these ecosystems.

A widely held—but rarely tested—hypothesis for the origin of animals is that they evolved from a unicellular ancestor, with an apical cilium surrounded by a microvillar collar, that structurally resembled modern sponge choanocytes and choanoflagellates 1 – 4 . Here we test this view of animal origins by comparing the transcriptomes, fates and behaviours of the three primary sponge cell types—choanocytes, pluripotent mesenchymal archaeocytes and epithelial pinacocytes—with choanoflagellates and other unicellular holozoans. Unexpectedly, we find that the transcriptome of sponge choanocytes is the least similar to the transcriptomes of choanoflagellates and is significantly enriched in genes unique to either animals or sponges alone. By contrast, pluripotent archaeocytes upregulate genes that control cell proliferation and gene expression, as in other metazoan stem cells and in the proliferating stages of two unicellular holozoans, including a colonial choanoflagellate. Choanocytes in the sponge Amphimedon queenslandica exist in a transient metastable state and readily transdifferentiate into archaeocytes, which can differentiate into a range of other cell types. These sponge cell-type conversions are similar to the temporal cell-state changes that occur in unicellular holozoans 5 . Together, these analyses argue against homology of sponge choanocytes and choanoflagellates, and the view that the first multicellular animals were simple balls of cells with limited capacity to differentiate. Instead, our results are consistent with the first animal cell being able to transition between multiple states in a manner similar to modern transdifferentiating and stem cells. Comparison of transcriptomes, cell fates and behaviour of three primary cell types from the sponge Amphimedon queenslandica with choanoflagellates and other unicellular holozoans suggests that the first animal cells transitioned between multiple states.

Biotic connectivity between ecosystems can provide major transport of organic matter and nutrients, influencing ecosystem structure and productivity 1 , yet the implications are poorly understood owing to human disruptions of natural flows 2 . When abundant, seabirds feeding in the open ocean transport large quantities of nutrients onto islands, enhancing the productivity of island fauna and flora 3 , 4 . Whether leaching of these nutrients back into the sea influences the productivity, structure and functioning of adjacent coral reef ecosystems is not known. Here we address this question using a rare natural experiment in the Chagos Archipelago, in which some islands are rat-infested and others are rat-free. We found that seabird densities and nitrogen deposition rates are 760 and 251 times higher, respectively, on islands where humans have not introduced rats. Consequently, rat-free islands had substantially higher nitrogen stable isotope (δ 15 N) values in soils and shrubs, reflecting pelagic nutrient sources. These higher values of δ 15 N were also apparent in macroalgae, filter-feeding sponges, turf algae and fish on adjacent coral reefs. Herbivorous damselfish on reefs adjacent to the rat-free islands grew faster, and fish communities had higher biomass across trophic feeding groups, with 48% greater overall biomass. Rates of two critical ecosystem functions, grazing and bioerosion, were 3.2 and 3.8 times higher, respectively, adjacent to rat-free islands. Collectively, these results reveal how rat introductions disrupt nutrient flows among pelagic, island and coral reef ecosystems. Thus, rat eradication on oceanic islands should be a high conservation priority as it is likely to benefit terrestrial ecosystems and enhance coral reef productivity and functioning by restoring seabird-derived nutrient subsidies from large areas of ocean. Productivity of coral reefs is enhanced near islands with no invasive rats, as populations of seabirds, which transfer nitrogen from deeper areas of ocean to the nearshore waters via their guano, are much larger than on rat-infested islands.

Most sponges have biomineralized spicules. Molecular clocks indicate sponge classes diverged in the Cryogenian, but the oldest spicules are Cambrian in age. Therefore, sponges either evolved spiculogenesis long after their divergences or Precambrian spicules were not amenable to fossilization. The former hypothesis predicts independent origins of spicules among sponge classes and presence of transitional forms with weakly biomineralized spicules, but this prediction has not been tested using paleontological data. Here, we report an early Cambrian sponge that, like several other early Paleozoic sponges, had weakly biomineralized and hexactine-based siliceous spicules with large axial filaments and high organic proportions. This material, along with Ediacaran microfossils containing putative non-biomineralized axial filaments, suggests that Precambrian sponges may have had weakly biomineralized spicules or lacked them altogether, hence their poor record. This work provides a new search image for Precambrian sponge fossils, which are critical to resolving the origin of sponge spiculogenesis and biomineralization. Sponge animals likely originated in the Precambrian, but their early spicular fossils are ambiguous. Here, Tang et al. report a new Cambrian sponge taxon with weakly biomineralized spicules and suggest that the poor Precambrian record may reflect the later evolution of biomineralization.