A late-Ediacaran crown-group sponge animal.

Sponges are the most basal metazoan phylum1 and may have played important roles in modulating the redox architecture of Neoproterozoic oceans2. Although molecular clocks predict that sponges diverged in the Neoproterozoic era3,4, their fossils have not been unequivocally demonstrated before the Cambrian period5-8, possibly because Precambrian sponges were aspiculate and non-biomineralized9. Here we describe a late-Ediacaran fossil, Helicolocellus cantori gen. et sp. nov., from the Dengying Formation (around 551-539 million years ago) of South China. This fossil is reconstructed as a large, stemmed benthic organism with a goblet-shaped body more than 0.4 m in height, with a body wall consisting of at least three orders of nested grids defined by quadrate fields, resembling a Cantor dust fractal pattern. The resulting lattice is interpreted as an organic skeleton comprising orthogonally arranged cruciform elements, architecturally similar to some hexactinellid sponges, although the latter are built with biomineralized spicules. A Bayesian phylogenetic analysis resolves H. cantori as a crown-group sponge related to the Hexactinellida. H. cantori confirms that sponges diverged and existed in the Precambrian as non-biomineralizing animals with an organic skeleton. Considering that siliceous biomineralization may have evolved independently among sponge classes10-13, we question the validity of biomineralized spicules as a necessary criterion for the identification of Precambrian sponge fossils.

Ancient gene linkages support ctenophores as sister to other animals.

A central question in evolutionary biology is whether sponges or ctenophores (comb jellies) are the sister group to all other animals. These alternative phylogenetic hypotheses imply different scenarios for the evolution of complex neural systems and other animal-specific traits1-6. Conventional phylogenetic approaches based on morphological characters and increasingly extensive gene sequence collections have not been able to definitively answer this question7-11. Here we develop chromosome-scale gene linkage, also known as synteny, as a phylogenetic character for resolving this question12. We report new chromosome-scale genomes for a ctenophore and two marine sponges, and for three unicellular relatives of animals (a choanoflagellate, a filasterean amoeba and an ichthyosporean) that serve as outgroups for phylogenetic analysis. We find ancient syntenies that are conserved between animals and their close unicellular relatives. Ctenophores and unicellular eukaryotes share ancestral metazoan patterns, whereas sponges, bilaterians, and cnidarians share derived chromosomal rearrangements. Conserved syntenic characters unite sponges with bilaterians, cnidarians, and placozoans in a monophyletic clade to the exclusion of ctenophores, placing ctenophores as the sister group to all other animals. The patterns of synteny shared by sponges, bilaterians, and cnidarians are the result of rare and irreversible chromosome fusion-and-mixing events that provide robust and unambiguous phylogenetic support for the ctenophore-sister hypothesis. These findings provide a new framework for resolving deep, recalcitrant phylogenetic problems and have implications for our understanding of animal evolution.

Extreme flow simulations reveal skeletal adaptations of deep-sea sponges.

Since its discovery1,2, the deep-sea glass sponge Euplectella aspergillum has attracted interest in its mechanical properties and beauty. Its skeletal system is composed of amorphous hydrated silica and is arranged in a highly regular and hierarchical cylindrical lattice that begets exceptional flexibility and resilience to damage3-6. Structural analyses dominate the literature, but hydrodynamic fields that surround and penetrate the sponge have remained largely unexplored. Here we address an unanswered question: whether, besides improving its mechanical properties, the skeletal motifs of E. aspergillum underlie the optimization of the flow physics within and beyond its body cavity. We use extreme flow simulations based on the 'lattice Boltzmann' method7, featuring over fifty billion grid points and spanning four spatial decades. These in silico experiments reproduce the hydrodynamic conditions on the deep-sea floor where E. aspergillum lives8-10. Our results indicate that the skeletal motifs reduce the overall hydrodynamic stress and support coherent internal recirculation patterns at low flow velocity. These patterns are arguably beneficial to the organism for selective filter feeding and sexual reproduction11,12. The present study reveals mechanisms of extraordinary adaptation to live in the abyss, paving the way towards further studies of this type at the intersection between fluid mechanics, organism biology and functional ecology.

Structural basis for piRNA targeting.

PIWI proteins use PIWI-interacting RNAs (piRNAs) to identify and silence transposable elements and thereby maintain genome integrity between metazoan generations1. The targeting of transposable elements by PIWI has been compared to mRNA target recognition by Argonaute proteins2,3, 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.

Possible poriferan body fossils in early Neoproterozoic microbial reefs.

Molecular phylogeny indicates that metazoans (animals) emerged early in the Neoproterozoic era1, but physical evidence is lacking. The search for animal fossils from the Proterozoic eon is hampered by uncertainty about what physical characteristics to expect. Sponges are the most basic known animal type2,3; it is possible that body fossils of hitherto-undiscovered Proterozoic metazoans might resemble aspect(s) of Phanerozoic fossil sponges. Vermiform microstructure4,5, a complex petrographic feature in Phanerozoic reefal and microbial carbonates, is now known to be the body fossil of nonspicular keratosan demosponges6-10. This Article presents petrographically identical vermiform microstructure from approximately 890-million-year-old reefs. The millimetric-to-centimetric vermiform-microstructured organism lived only on, in and immediately beside reefs built by calcifying cyanobacteria (photosynthesizers), and occupied microniches in which these calcimicrobes could not live. If vermiform microstructure is in fact the fossilized tissue of keratose sponges, the material described here would represent the oldest body-fossil evidence of animals known to date, and would provide the first physical evidence that animals emerged before the Neoproterozoic oxygenation event and survived through the glacial episodes of the Cryogenian period.

Marine sponge microbe provides insights into evolution and virulence of the tubercle bacillus.

Reconstructing the evolutionary origins of Mycobacterium tuberculosis, the causative agent of human tuberculosis, has helped identify bacterial factors that have led to the tubercle bacillus becoming such a formidable human pathogen. Here we report the discovery and detailed characterization of an exceedingly slow growing mycobacterium that is closely related to M. tuberculosis for which we have proposed the species name Mycobacterium spongiae sp. nov., (strain ID: FSD4b-SM). The bacterium was isolated from a marine sponge, taken from the waters of the Great Barrier Reef in Queensland, Australia. Comparative genomics revealed that, after the opportunistic human pathogen Mycobacterium decipiens, M. spongiae is the most closely related species to the M. tuberculosis complex reported to date, with 80% shared average nucleotide identity and extensive conservation of key M. tuberculosis virulence factors, including intact ESX secretion systems and associated effectors. Proteomic and lipidomic analyses showed that these conserved systems are functional in FSD4b-SM, but that it also produces cell wall lipids not previously reported in mycobacteria. We investigated the virulence potential of FSD4b-SM in mice and found that, while the bacteria persist in lungs for 56 days after intranasal infection, no overt pathology was detected. The similarities with M. tuberculosis, together with its lack of virulence, motivated us to investigate the potential of FSD4b-SM as a vaccine strain and as a genetic donor of the ESX-1 genetic locus to improve BCG immunogenicity. However, neither of these approaches resulted in superior protection against M. tuberculosis challenge compared to BCG vaccination alone. The discovery of M. spongiae adds to our understanding of the emergence of the M. tuberculosis complex and it will be another useful resource to refine our understanding of the factors that shaped the evolution and pathogenesis of M. tuberculosis.

Cellular migration into a subretinal honeycomb-shaped prosthesis for high-resolution prosthetic vision.

In patients blinded by geographic atrophy, a subretinal photovoltaic implant with 100 µm pixels provided visual acuity closely matching the pixel pitch. However, such flat bipolar pixels cannot be scaled below 75 µm, limiting the attainable visual acuity. This limitation can be overcome by shaping the electric field with 3-dimensional (3-D) electrodes. In particular, elevating the return electrode on top of the honeycomb-shaped vertical walls surrounding each pixel extends the electric field vertically and decouples its penetration into tissue from the pixel width. This approach relies on migration of the retinal cells into the honeycomb wells. Here, we demonstrate that majority of the inner retinal neurons migrate into the 25 µm deep wells, leaving the third-order neurons, such as amacrine and ganglion cells, outside. This enables selective stimulation of the second-order neurons inside the wells, thus preserving the intraretinal signal processing in prosthetic vision. Comparable glial response to that with flat implants suggests that migration and separation of the retinal cells by the walls does not cause additional stress. Furthermore, retinal migration into the honeycombs does not negatively affect its electrical excitability, while grating acuity matches the pixel pitch down to 40 µm and reaches the 27 µm limit of natural resolution in rats with 20 µm pixels. These findings pave the way for 3-D subretinal prostheses with pixel sizes of cellular dimensions.

Terpene biosynthesis in marine sponge animals.

Sea sponges are the largest marine source of small-molecule natural products described to date. Sponge-derived molecules, such as the chemotherapeutic eribulin, the calcium-channel blocker manoalide, and antimalarial compound kalihinol A, are renowned for their impressive medicinal, chemical, and biological properties. Sponges contain microbiomes that control the production of many natural products isolated from these marine invertebrates. In fact, all genomic studies to date investigating the metabolic origins of sponge-derived small molecules concluded that microbes-not the sponge animal host-are the biosynthetic producers. However, early cell-sorting studies suggested the sponge animal host may play a role particularly in the production of terpenoid molecules. To investigate the genetic underpinnings of sponge terpenoid biosynthesis, we sequenced the metagenome and transcriptome of an isonitrile sesquiterpenoid-containing sponge of the order Bubarida. Using bioinformatic searches and biochemical validation, we identified a group of type I terpene synthases (TSs) from this sponge and multiple other species, the first of this enzyme class characterized from the sponge holobiome. The Bubarida TS-associated contigs consist of intron-containing genes homologous to sponge genes and feature GC percentage and coverage consistent with other eukaryotic sequences. We identified and characterized TS homologs from five different sponge species isolated from geographically distant locations, thereby suggesting a broad distribution amongst sponges. This work sheds light on the role of sponges in secondary metabolite production and speaks to the possibility that other sponge-specific molecules originate from the animal host.

Getting Nervous: An Evolutionary Overhaul for Communication.

The evolution of a nervous system as a control system of the body's functions is a key innovation of animals. Its fundamental units are neurons, highly specialized cells dedicated to fast cell-cell communication. Neurons pass signals to other neurons, muscle cells, or gland cells at specialized junctions, the synapses, where transmitters are released from vesicles in a Ca2+-dependent fashion to activate receptors in the membrane of the target cell. Reconstructing the origins of neuronal communication out of a more simple process remains a central challenge in biology. Recent genomic comparisons have revealed that all animals, including the nerveless poriferans and placozoans, share a basic set of genes for neuronal communication. This suggests that the first animal, the Urmetazoan, was already endowed with neurosecretory cells that probably started to connect into neuronal networks soon afterward. Here, we discuss scenarios for this pivotal transition in animal evolution.

Pluripotency and the origin of animal multicellularity.

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 choanoflagellates1-4. 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 holozoans5. 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.

Transcriptomic responses of Mediterranean sponges upon encounter with symbiont microbial consortia.

BACKGROUND: Sponges (phylum Porifera) constantly interact with microbes. They graze on microbes from the water column by filter-feeding and they harbor symbiotic partners within their bodies. In experimental setups, sponges take up symbionts at lower rates compared with seawater microbes. This suggests that sponges have the capacity to differentiate between microbes and preferentially graze in non-symbiotic microbes, although the underlying mechanisms of discrimination are still poorly understood. Genomic studies showed that, compared to other animal groups, sponges present an extended repertoire of immune receptors, in particular NLRs, SRCRs, and GPCRs, and a handful of experiments showed that sponges regulate the expression of these receptors upon encounter with microbial elicitors. We hypothesize that sponges may rely on differential expression of their diverse repertoire of poriferan immune receptors to sense different microbial consortia while filter-feeding. To test this, we characterized the transcriptomic response of two sponge species, Aplysina aerophoba and Dysidea avara, upon incubation with microbial consortia extracted from A. aerophoba in comparison with incubation with seawater microbes. The sponges were sampled after 1 h, 3 h, and 5 h for RNA-Seq differential gene expression analysis. RESULTS: D. avara incubated with A. aerophoba-symbionts regulated the expression of genes related to immunity, ubiquitination, and signaling. Within the set of differentially-expressed immune genes we identified different families of Nucleotide Oligomerization Domain (NOD)-Like Receptors (NLRs). These results represent the first experimental evidence that different types of NLRs are involved in microbial discrimination in a sponge. In contrast, the transcriptomic response of A. aerophoba to its own symbionts involved comparatively fewer genes and lacked genes encoding for immune receptors. CONCLUSION: Our work suggests that: (i) the transcriptomic response of sponges upon microbial exposure may imply "fine-tuning" of baseline gene expression as a result of their interaction with microbes, (ii) the differential response of sponges to microbial encounters varied between the species, probably due to species-specific characteristics or related to host's traits, and (iii) immune receptors belonging to different families of NLR-like genes played a role in the differential response to microbes, whether symbionts or food bacteria. The regulation of these receptors in sponges provides further evidence of the potential role of NLRs in invertebrate host-microbe interactions. The study of sponge responses to microbes exemplifies how investigating different animal groups broadens our knowledge of the evolution of immune specificity and symbiosis.

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 influence animal development. Here, we show that the loss of a key photosymbiont (i.e., bleaching) upon shading correlates with a stark body-plan reorganization in the common aquarium cyanosponge Lendenfeldia chondrodes. The morphological changes observed in shaded sponges include the development of a thread-like morphology that contrasts with the flattened, foliose morphology of control specimens. The microanatomy of shaded sponges markedly differed from that of control sponges, with shaded specimens lacking a well-developed cortex and choanosome. Also, the palisade of polyvacuolar gland-like cells typical in control specimens was absent in shaded sponges. The morphological changes observed in shaded specimens are coupled with broad transcriptomic changes and include the modulation of signaling pathways involved in animal morphogenesis and immune response, such as the Wnt, transforming growth factor ß (TGF-ß), and TLR-ILR pathways. This study provides a genetic, physiological, and morphological assessment of the effect of microbiome changes on sponge postembryonic development and homeostasis. The correlated response of the sponge host to the collapse of the population of symbiotic cyanobacteria provides evidence for a coupling between the sponge transcriptomic state and the state of its microbiome. This coupling suggests that the ability of animals to interact with their microbiomes and respond to microbiome perturbations has deep evolutionary origins in this group.

Hot off the press.

A personal selection of 32 recent papers is presented covering various aspects of current developments in bioorganic chemistry and novel natural products such as nitidane from Heteromurus nitidus.

Comparative genomics identifies key adaptive traits of sponge-associated microbial symbionts.

Sponge microbiomes are often highly diverse making it difficult to determine which lineages are important for maintaining host health and homeostasis. Characterising genomic traits associated with symbiosis can improve our knowledge of which lineages have adapted to their host and what functions they might provide. Here we examined five microbial families associated with sponges that have previously shown evidence of cophylogeny, including Endozoicomonadaceae, Nitrosopumilaceae, Spirochaetaceae, Microtrichaceae and Thermoanaerobaculaceae, to better understand the mechanisms behind their symbiosis. We compared sponge-associated genomes to genomes found in other environments and found that sponge-specific clades were enriched in genes encoding many known mechanisms for symbiont survival, such as avoiding phagocytosis and defence against foreign genetic elements. We expand on previous knowledge to show that glycosyl hydrolases with sulfatases and sulfotransferases likely form multienzyme degradation pathways to break and remodel sulfated polysaccharides and reveal an enrichment in superoxide dismutase that may prevent damage from free oxygen radicals produced by the host. Finally, we identified novel traits in sponge-associated symbionts, such as urea metabolism in Spirochaetaceae which was previously shown to be rare in the phylum Spirochaetota. These results identify putative mechanisms by which symbionts have adapted to living in association with sponges.

Diversity and structure of the deep-sea sponge microbiome in the equatorial Atlantic Ocean.

Sponges (phylum Porifera) harbour specific microbial communities that drive the ecology and evolution of the host. Understanding the structure and dynamics of these communities is emerging as a primary focus in marine microbial ecology research. Much of the work to date has focused on sponges from warm and shallow coastal waters, while sponges from the deep ocean remain less well studied. Here, we present a metataxonomic analysis of the microbial consortia associated with 23 individual deep-sea sponges. We identify a high abundance of archaea relative to bacteria across these communities, with certain sponge microbiomes comprising more than 90 % archaea. Specifically, the archaeal family Nitrosopumilaceae is prolific, comprising over 99 % of all archaeal reads. Our analysis revealed that sponge microbial communities reflect the host sponge phylogeny, indicating a key role for host taxonomy in defining microbiome composition. Our work confirms the contribution of both evolutionary and environmental processes to the composition of microbial communities in deep-sea sponges.

Natural Products That Contain Higher Homologated Amino Acids.

This review focuses on discussing natural products (NPs) that contain higher homologated amino acids (homoAAs) in the structure as well as the proposed and characterized biosynthesis of these non-proteinogenic amino acids. Homologation of amino acids includes the insertion of a methylene group into its side chain. It is not a very common modification found in NP biosynthesis as approximately 450 homoAA-containing NPs have been isolated from four bacterial phyla (Cyanobacteria, Actinomycetota, Myxococcota, and Pseudomonadota), two fungal phyla (Ascomycota and Basidiomycota), and one animal phylum (Porifera), except for a few examples. Amino acids that are found to be homologated and incorporated in the NP structures include the following ten amino acids: alanine, arginine, cysteine, isoleucine, glutamic acid, leucine, phenylalanine, proline, serine, and tyrosine, where isoleucine, leucine, phenylalanine, and tyrosine share the comparable enzymatic pathway. Other amino acids have their individual homologation pathway (arginine, proline, and glutamic acid for bacteria), likely utilize the primary metabolic pathway (alanine and glutamic acid for fungi), or have not been reported (cysteine and serine). Despite its possible high potential in the drug discovery field, the biosynthesis of homologated amino acids has a large room to explore for future combinatorial biosynthesis and metabolic engineering purpose.

Metagenomic mining of two Egyptian Red Sea sponges associated microbial community.

The Red Sea is a promising habitat for the discovery of new bioactive marine natural products. Sponges associated microorganisms represent a wealthy source of compounds with unique chemical structures and diverse biological activities. Metagenomics is an important omics-based culture-independent technique that is used as an effective tool to get genomic and functional information on sponge symbionts. In this study, we used metagenomic analysis of two Egyptian Red Sea sponges Hyrtios erectus and Phorbas topsenti microbiomes to study the biodiversity and the biosynthetic potential of the Red Sea sponges to produce bioactive compounds. Our data revealed high biodiversity of the two sponges' microbiota with phylum Proteobacteria as the most dominant phylum in the associated microbial community with an average of 31% and 70% respectively. The analysis also revealed high biosynthetic potential of sponge Hyrtios erectus microbiome through detecting diverse types of biosynthetic gene clusters (BGCs) with predicted cytotoxic, antibacterial and inhibitory action. Most of these BGCs were predicted to be novel as they did not show any similarity with any MIBiG database known cluster. This study highlights the importance of the microbiome of the collected Red Sea sponge Hyrtios erectus as a valuable source of new bioactive natural products.

Phylosymbiosis and metabolomics resolve phenotypically plastic and cryptic sponge species in the genus Agelas across the Caribbean basin.

Fundamental to holobiont biology is recognising how variation in microbial composition and function relates to host phenotypic variation. Sponges often exhibit considerable phenotypic plasticity and also harbour dense microbial communities that function to protect and nourish hosts. One of the most prominent sponge genera on Caribbean coral reefs is Agelas. Using a comprehensive set of morphological (growth form, spicule), chemical and molecular data on 13 recognised species of Agelas in the Caribbean basin, we were able to define only five species (=clades) and found that many morphospecies designations were incongruent with phylogenomic and population genetic analyses. Microbial communities were also strongly differentiated between phylogenetic species, showing little evidence of cryptic divergence and relatively low correlation with morphospecies assignment. Metagenomic analyses also showed strong correspondence to phylogenetic species, and to a lesser extent, geographical and morphological characters. Surprisingly, the variation in secondary metabolites produced by sponge holobionts was explained by geography and morphospecies assignment, in addition to phylogenetic species, and covaried significantly with a subset of microbial symbionts. Spicule characteristics were highly plastic, under greater impact from geographical location than phylogeny. Our results suggest that while phenotypic plasticity is rampant in Agelas, morphological differences within phylogenetic species affect functionally important ecological traits, including the composition of the symbiotic microbial communities and metabolomic profiles.

Bioemulsifier from sponge-associated bacteria reduces staphylococcal biofilm.

Biofilm formation is a major health concern and studies have been pursued to find compounds able to prevent biofilm establishment and remove pre-existing biofilms. While biosurfactants (BS) have been well-known for possessing antibiofilm activities, bioemulsifiers (BE) are still scarcely explored for this purpose. The present study aimed to evaluate the bioemulsifying properties of cell-free supernatants produced by Bacillaceae and Vibrio strains isolated from marine sponges and investigate their antiadhesive and antibiofilm activities against different pathogenic Gram-positive and Gram-negative bacteria. The BE production by the marine strains was confirmed by the emulsion test, drop-collapsing, oil-displacement, cell hydrophobicity and hemolysis assays. Notably, Bacillus cereus 64BHI1101 displayed remarkable emulsifying activity and the ultrastructure analysis of its BE extract (BE64-1) revealed the presence of structures typically observed in macromolecules composed of polysaccharides and proteins. BE64-1 showed notable antiadhesive and antibiofilm activities against Staphylococcus aureus, with a reduction of adherence of up to 100 % and a dispersion of biofilm of 80 %, without affecting its growth. BE64-1 also showed inhibition of Staphylococcus epidermidis and Escherichia coli biofilm formation and adhesion. Thus, this study provides a starting point for exploring the antiadhesive and antibiofilm activities of BE from sponge-associated bacteria, which could serve as a valuable tool for future research to combat S. aureus biofilms.

Marine heatwave-driven mass mortality and microbial community reorganisation in an ecologically important temperate sponge.

Marine heatwaves (MHWs) are increasing in frequency, duration and intensity, disrupting global marine ecosystems. While most reported impacts have been in tropical areas, New Zealand experienced its strongest and longest MHW in 2022, profoundly affecting marine sponges. Sponges are vital to rocky benthic marine communities, with their abundance influencing ecosystem functioning. This study examines the impact of this MHW on the photosynthetic sponge Cymbastella lamellata in Fiordland, New Zealand. We describe the extent, physiological responses, mortality, microbial community changes and ecological impact of this MHW on C. lamellata. The Fiordland MHW reached a maximum temperature of 4.4°C above average, lasting for 259 days. Bleaching occurred in >90% of the C. lamellata Fiordland population. The population size exceeded 66 million from 5 to 25 m, making this the largest bleaching event of its kind ever recorded. We identified the photosynthetic symbiont as a diatom, and bleached sponges had reduced photosynthetic efficiency. Post-MHW surveys in 2023 found that over 50% of sponges at sampling sites had died but that the remaining sponges had mostly recovered from earlier bleaching. Using a simulated MHW experiment, we found that temperature stress was a driver of necrosis rather than bleaching, despite necrosis only rarely being observed in the field (<2% of sponges). This suggests that bleaching may not be the cause of the mortality directly. We also identified a microbial community shift in surviving sponges, which we propose represents a microbial-mediated adaptive response to MHWs. We also found that C. lamellata are key contributors of dissolved organic carbon to the water column, with their loss likely impacting ecosystem function. We demonstrate the potential for MHWs to disrupt key marine phyla in temperate regions, highlighting how susceptible temperate sponges globally might be to MHWs.