Description: We report and describe new material of streptaster-bearing Astrophorida sponges collected in Norway: Characellapachastrelloides, Pachastrella nodulosa sp. nov., Poecillastra compressa, Vulcanella cf. aberrans, Thenea abyssorum,Thenea levis, Thenea muricata and Thenea valdiviae. Because many of these species were described in the end of the 19thcentury their original descriptions are often incomplete. The Norwegian specimens are the basis for a revision of themorphology, taxonomy and distribution of these species. These are the first records of C. pachastrelloides and V. cf.aberrans from the Norwegian coast. Pachastrella nodulosa sp. nov. differs from Pachastrella monilifera by (i) its knobbysurface and (ii) the absence of large oxeas, (iii) its amphiasters have on average less actines and are less spiny, finally (iv)microxeas are rare and with a distinct morphology (although there is some doubt concerning their origin). In the presentstudy, Characella tuberosa (from South Africa), Pachastrella abyssi (from the North-West Atlantic) and Thenea schmidti(from the North-East Atlantic) are resurrected. To help their future identifications, all the Norwegian species describedwere associated with DNA barcodes: a cytochrome c oxidase subunit I (COI) gene partial fragment and/or a 28S ribosomalgene partial fragment (C1–D2 domains). Furthermore, a key to the streptaster-bearing Astrophorida of the North-East Atlantic and the Mediterranean Sea is also given (lithistids not included).Nous signalons la présence et décrivons des spécimens d’Astrophorida à streptasters nouvellement récoltés en Norvège:Characella pachastrelloides, Pachastrella nodulosa sp. nov., Poecillastra compressa, Vulcanella cf. aberrans, Theneaabyssorum, Thenea levis, Thenea muricata et Thenea valdiviae. Plusieurs de ces espèces ont été décrites de manièreincomplète à la fin du 19ème siècle. Les spécimens norvégiens sont l’occasion de réviser la morphologie, la taxonomie etla distribution de ces espèces. C’est la première fois que C. pachastrelloides et V. cf. aberrans sont mentionnés sur la côtenorvégienne. Pachastrella nodulosa sp. nov. se distingue de Pachastrella monilifera par (i) sa surface noduleuse et (ii)l’absence de grands oxes, (iii) ses amphiasters ont en moyenne moins d’actines et sont moins épineux, enfin (iv) lesmicroxes sont rares et ont une morphologie distincte (bien qu’il y ait encore des doutes sur leur origine). Au cours de notreétude, Characella tuberosa (d’Afrique du Sud), Pachastrella abyssi (de l’Atlantique Nord-Ouest) et Thenea schmidti (del’Atlantique Nord-Est) sont ressuscités. Afin d’aider leurs identifications futures, toutes les espèces de Norvège décritesont été associées à des code-barres moléculaires: un fragment partiel du gène de la sous-unité I du cytochrome c oxydase(COI) et/ou un fragment partiel du gène ribosomique 28S (domaines C1-D2). De plus, une clé pour identifier les Astrophorida à streptasters de l’Atlantique Nord-Est et de Méditerrannée est également fournie (lithistides non inclus).

Description: Geodia species north of 60°N in the Atlantic appeared in the literature for the first time when Bowerbank described Geodia barretti and G. macandrewii in 1858 from western Norway. Since then, a number of species have been based on material from various parts of the region: G. simplex, Isops phlegraei, I. pallida, I. sphaeroides, Synops pyriformis, G. parva, G. normani, G. atlantica, Sidonops mesotriaena (now called G. hentscheli), and G. simplicissima. In addition to these 12 nominal species, four species described from elsewhere are claimed to have been identified in material from the northeast Atlantic, namely G. nodastrella and G. cydonium (and its synonyms Cydonium muelleri and Geodia gigas ). In this paper, we revise the boreo-arctic Geodia species using morphological, molecular, and biogeographical data. We notably compare northwest and northeast Atlantic specimens. Biological data (reproduction, biochemistry, microbiology, epibionts) for each species are also reviewed. Our results show that there are six valid species of boreo-arctic Atlantic Geodia while other names are synonyms or mis-identifications. Geodia barretti, G. atlantica, G. macandrewii, and G. hentscheli are well established and widely distributed. The same goes for Geodia phlegraei, but this species shows a striking geographical and bathymetric variation, which led us to recognize two species, G. phlegraei and G. parva(here resurrected). Some Geodia are arctic species (G. hentscheli, G. parva), while others are typically boreal (G. atlantica, G. barretti, G. phlegraei , G. macandrewii). No morphological differences were found between specimens from the northeast and northwest Atlantic, except for G. parva . The Folmer cytochrome oxidase subunit I (COI) fragment is unique for every species and invariable over their whole distribution range, except for G. barretti which had two haplotypes. 18S is unique for four species but cannot discriminate G. phlegraei and G. parva. Two keys to the boreo-arctic Geodia are included, one based on external morphology, the other based on spicule morphology.

Description: Cold-water coral reefs are known to locally enhance the diversity of deep-sea fauna as well as of microbes. Sponges are among the most diverse faunal groups in these ecosystems, and many of them host large abundances of microbes in their tissues. In this study, twelve sponge species from three cold-water coral reefs off Norway were investigated for the relationship between sponge phylogenetic classification (species and family level), as well as sponge type (high versus low microbial abundance), and the diversity of sponge-associated bacterial communities, taking also geographic location and water depth into account. Community analysis by Automated Ribosomal Intergenic Spacer Analysis (ARISA) showed that as many as 345 (79%) of the 437 different bacterial operational taxonomic units (OTUs) detected in the dataset were shared between sponges and sediments, while only 70 (16%) appeared purely sponge-associated. Furthermore, changes in bacterial community structure were significantly related to sponge species (63% of explained community variation), sponge family (52%) or sponge type (30%), whereas mesoscale geographic distances and water depth showed comparatively small effects (〈5% each). In addition, a highly significant, positive relationship between bacterial community dissimilarity and sponge phylogenetic distance was observed within the ancient family of the Geodiidae. Overall, the high diversity of sponges in cold-water coral reefs, combined with the observed sponge-related variation in bacterial community structure, support the idea that sponges represent heterogeneous, yet structured microbial habitats that contribute significantly to enhancing bacterial diversity in deep-sea ecosystems.

Description: Seamounts represent ideal systems to study the influence and interdependency of environmental gradients at a single geographic location. These topographic features represent a prominent habitat for various forms of life, including microbiota and macrobiota, spanning benthic as well as pelagic organisms. While it is known that seamounts are globally abundant structures, it still remains unclear how and to which extent the complexity of the sea floor is intertwined with the local oceanographic mosaic, biogeochemistry, and microbiology of a seamount ecosystem. Along these lines, the present study aimed to explore whether and to what extent seamounts can have an imprint on the microbial community composition of seawater and of sessile benthic invertebrates, sponges. For our high-resolution sampling approach of microbial diversity (16S rRNA gene amplicon sequencing) along with measurements of inorganic nutrients and other biogeochemical parameters, we focused on the Schulz Bank seamount ecosystem, a sponge ground ecosystem which is located on the Arctic Mid-Ocean Ridge. Seawater samples were collected at two sampling depths (mid-water, MW, and near-bed water, BW) from a total of 19 sampling sites. With a clustering approach we defined microbial microhabitats within the pelagic realm at Schulz Bank, which were mapped onto the seamount's topography and related to various environmental parameters (such as suspended particulate matter, SPM; dissolved inorganic carbon, DIC; silicate, SiO−4; phosphate, PO3−4; ammonia, NH+4; nitrate, NO2−3; nitrite, NO−2; depth; and dissolved oxygen, O2). The results of our study reveal a “seamount effect” (sensu stricto) on the microbial mid-water pelagic community at least 200 m above the sea floor. Further, we observed a strong spatial heterogeneity in the pelagic microbial landscape across the seamount, with planktonic microbial communities reflecting oscillatory and circulatory water movements, as well as processes of bentho-pelagic coupling. Depth, NO2−3, SiO−4, and O2 concentrations differed significantly between the determined pelagic microbial clusters close to the sea floor (BW), suggesting that these parameters were presumably linked to changes in microbial community structures. Secondly, we assessed the associated microbial community compositions of three sponge species along a depth gradient of the seamount. While sponge-associated microbial communities were found to be mainly species-specific, we also detected significant intra-specific differences between individuals, depending on the pelagic near-bed cluster they originated from. The variable microbial phyla (i.e. phyla which showed significant differences across varying depth, NO2−3, SiO−4, O2 concentrations, and different from local seawater communities) were distinct for every sponge species when considering average abundances per species. Variable microbial phyla included representatives of both those taxa traditionally counted for the variable community fraction and taxa counted traditionally for the core community fraction. Microbial co-occurrence patterns for the three examined sponge species Geodia hentscheli, Lissodendoryx complicata, and Schaudinnia rosea were distinct from each other. Over all, this study shows that topographic structures such as the Schulz Bank seamount can have an imprint (seamount effect sensu lato) on both the microbial community composition of seawater and sessile benthic invertebrates such as sponges by an interplay between the geology, physical oceanography, biogeochemistry, and microbiology of seamounts.

Description: Hexactinellid sponges are common in the deep sea, but their functional integration into those ecosystems remains poorly understood. The phylogenetically related species Schaudinnia rosea and Vazella pourtalesii were herein incubated for nitrogen and phosphorous, returning markedly different nutrient fluxes. Transmission electron microscopy (TEM) revealed S. rosea to host a low abundance of extracellular microbes, while Vazella pourtalesii showed higher microbial abundance and hosted most microbes within bacteriosyncytia, a novel feature for Hexactinellida. Amplicon sequences of the microbiome corroborated large between-species differences, also between the sponges and the seawater of their habitats. Metagenome-assembled genome of the V. pourtalesii microbiota revealed genes coding for enzymes operating in nitrification, denitrification, dissimilatory nitrate reduction to ammonium, nitrogen fixation, and ammonia/ammonium assimilation. In the nitrification and denitrification pathways some enzymes were missing, but alternative bridging routes allow the microbiota to close a N cycle in the holobiont. Interconnections between aerobic and anaerobic pathways may facilitate the sponges to withstand the low-oxygen conditions of deep-sea habitats. Importantly, various N pathways coupled to generate ammonium, which, through assimilation, fosters the growth of the sponge microbiota. TEM showed that the farmed microbiota is digested by the sponge cells, becoming an internal food source. This microbial farming demands more ammonium that can be provided internally by the host sponges and some 2.6 million kg of ammonium from the seawater become annually consumed by the aggregations of V. pourtalesii. Such ammonium removal is likely impairing the development of the free-living bacterioplankton and the survival chances of other sponge species that feed on bacterioplankton. Such nutritional competitive exclusion would favor the monospecific character of the V. pourtalesii aggregations. These aggregations also affect the surrounding environment through an annual release of 27.3 million kg of nitrite and, in smaller quantities, of nitrate and phosphate. The complex metabolic integration among the microbiota and the sponge suggests that the holobiont depends critically on the correct functioning of its N-driven microbial engine. The metabolic intertwining is so delicate that it changed after moving the sponges out of their habitat for a few days, a serious warning on the conservation needs of these sponge aggregations.

Description: 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.

Description: Sponges are ubiquitous components of various deep‐sea habitats, including cold water coral reefs, and form deep‐sea sponge grounds. Although the deep sea is generally considered to be a food‐limited environment, these ecosystems are known to be hotspots of biodiversity and carbon cycling. To assess the role of sponges in the carbon cycling of deep‐sea ecosystems, we studied the carbon budgets of six dominant deep‐sea sponges of different phylogenetic origin, with various growth forms and hosting distinct associated microbial communities, in an ex situ aquarium setup. Additionally, we determined biomass metrics—planar surface area, volume, wet weight, dry weight (DW), ash‐free dry weight, and organic carbon (C) content—and conversion factors for all species. Oxygen (O2) removal rates averaged 3.3 ± 2.8 μmol O2 g DWsponge h−1 (mean ± SD), live particulate (bacterio‐ and phytoplankton) organic carbon removal rates averaged 0.30 ± 0.39 μmol C g DWsponge h−1 and dissolved organic carbon (DOC) removal rates averaged 18.70 ± 25.02 μmol C g DWsponge h−1. Carbon mass balances were calculated for four species and revealed that the sponges acquired 1.3–6.6 times the amount of carbon needed to sustain their minimal respiratory demands. These results indicate that irrespective of taxonomic class, growth form, and abundance of microbial symbionts, DOC is responsible for over 90% of the total net organic carbon removal of deep‐sea sponges and allows them to sustain themselves in otherwise food‐limited environments on the ocean floor.

Description: Highlights: • First time hybridization is detected in deep-water sponges (Phakellia) using SNPs. • Hybridization corroborated by morphological and microbial analyses. • Connectivity between shallow populations of Phakellia robusta spanning ca. 2,000 km. • Molecular connectivity explained by prevalent oceanographic currents. Abstract: Deep-sea North Atlantic sponge grounds are crucial components of the marine fauna providing a key role in ecosystem functioning. To properly develop effective conservation and management plans, it is crucial to understand the genetic diversity, molecular connectivity patterns and turnover at the population level of the species involved. Here we present the study of two congeneric sponges, Phakellia robusta and Phakellia hirondellei, using multiple sources of evidence. Our phylogenetic study using a fragment of COI placed these two species as sister. Haplotype network analysis using COI revealed no genetic structure for P. hirondellei in samples from the Cantabrian Sea (〈100 km). Contrastingly, P. robusta showed a clear genetic structure separating deep-water samples from the Cantabrian Sea and the Hatton-Rockall Basin, from samples from shallower waters from Kerry Head Reefs, NW of Orkney, and Norway. ddRADSeq-derived SNPs for P. robusta also segregated samples by bathymetry rather than by geographical distances, and detected a predominant northwards migration for shallow-water specimens connecting sites separated ca. 2,000 km, probably thanks to prevalent oceanographic currents. Importantly, our analysis using SNPs combining the datasets of the two species revealed the presence of potential hybrids, which was corroborated by morphological (spicule) and microbial (16S amplicon sequencing) analyses. Our data suggest that hybridization between these two species occurred at least two times in the past. We discuss the importance of using next-generation techniques to unveil hybridization and the implications of our results for conservation.

Description: In 2016, the research ice-breaker Polarstern surveyed the submerged peaks of the permanently ice-covered Langseth Ridge, a tectonic feature comprising the Karasik seamount and two deeper seamount peaks, abutting the Gakkel ultra-slow spreading ridge (87°N 62°E to 85.5°N 57.4°E)1. A towed marine camera sled and a hybrid remotely operated vehicle revealed these peaks to be covered by a dense demosponge community, at first glance reminiscent of North Atlantic Geodia grounds (sensu2). Sponges were observed on top of a thick layer of spicule mat (Figure 1 and Video S1), intermixed with underlying layers of empty siboglinid tubes and bivalve shells, a substrate covering almost the entire seafloor. We observed trails of densely interwoven spicules connected directly to the underside or lower flanks of sponge individuals (Figure 1), suggesting these trails are traces of motile sponges. This is the first time abundant sponge trails have been observed in situ and attributed to sponge mobility. Given the low primary production in this permanently ice-covered region, these trails may relate to feeding behavior and/or a strategy for dispersal of juveniles. Such trails may remain visible for long periods given the regionally low sedimentation rates.

Description: Little is known about dispersal in deep-sea ecosystems, especially for sponges, which are abundant ecosystem engineers. Understanding patterns of gene flow in deep-sea sponges is essential, especially in areas where rising pressure from anthropogenic activities makes difficult to combine management and conservation. Here, we combined population genomics and oceanographic modelling to understand how Northeast Atlantic populations (Cantabrian Sea to Norway) of the deep-sea sponge Phakellia ventilabrum are connected. The analysis comprised ddRADseq derived SNP datasets of 166 individuals collected from 57 sampling stations from 17 different areas, including two Marine Protected Areas, one Special Area of Conservation and other areas with different levels of protection. The 4,017 neutral SNPs used indicated high connectivity and panmixis amongst the majority of areas (Ireland to Norway), spanning ca. 2,500-km at depths of 99–900 m. This was likely due to the presence of strong ocean currents allowing long-distance larval transport, as supported by our migration analysis and by 3D particle tracking modelling. On the contrary, the Cantabrian Sea and Roscoff (France) samples, the southernmost areas in our study, appeared disconnected from the remaining areas, probably due to prevailing current circulation patterns and topographic features, which might be acting as barriers for gene flow. Despite this major genetic break, our results suggest that all protected areas studied are well-connected with each other. Interestingly, analysis of SNPs under selection replicated results obtained for neutral SNPs. The relatively low genetic diversity observed along the study area, though, highlights the potential fragility of this species to changing climates, which might compromise resilience to future threats.