ALBERT

Description: Benthic fauna refers to all fauna that live in or on the seafloor, which researchers typically divide into size classes meiobenthos (32/64 µm–0.5/1 mm), macrobenthos (250 µm–1 cm), and megabenthos (〉1 cm). Benthic fauna play important roles in bioturbation activity, mineralization of organic matter, and in marine food webs. Evaluating their role in these ecosystem functions requires knowledge of their global distribution and biomass. We therefore established the BenBioDen database, the largest open-access database for marine benthic biomass and density data compiled so far. In total, it includes 11,792 georeferenced benthic biomass and 51,559 benthic density records from 384 and 600 studies, respectively. We selected all references following the procedure for systematic reviews and meta-analyses, and report biomass records as grams of wet mass, dry mass, or ash-free dry mass, or carbon per m2 and as abundance records as individuals per m2. This database provides a point of reference for future studies on the distribution and biomass of benthic fauna.

Description: Establishment of adequate conservation areas represents a challenging but crucial task in the conservation of genetic diversity and biological variability. Anthropogenic pressures on marine ecosystems and organisms are steadily increasing. Whether and to what extent these pressures influence marine genetic biodiversity is only starting to be revealed. Using 16S rRNA gene amplicon sequencing, we analysed the microbial community structure of 33 individuals of the habitat-forming glass sponge Vazella pourtalesii, as well as reference seawater, sediment, and biofilm samples. We assessed how two anthropogenic impacts, i.e. habitat destruction by trawling and artificial substrate provision (moorings made of composite plastic), correspond with in situ V. pourtalesii microbiome variability. In addition, we evaluated the role of two bottom fishery closures in preserving sponge-associated microbial diversity on the Scotian Shelf, Canada. Our results illustrate that V. pourtalesii sponges collected from pristine sites within fishery closures contained distinct and taxonomically largely novel microbial communities. At the trawled site we recorded significant quantitative differences in distinct microbial phyla, such as a reduction in Nitrospinae in sponges and environmental references. Individuals of V. pourtalesii growing on the mooring were significantly enriched in Bacteroidetes, Verrucomicrobia and Cyanobacteria in comparison to sponge individuals growing on the natural seabed. Due to a concomitant enrichment of these taxa in the mooring biofilm, we propose that biofilms on artificial substrates may ‘prime’ sponge-associated microbial communities when small sponges settle on such substrates. These observations likely have relevant management implications when considering the increase of artificial substrates in the marine environment, e.g., marine litter, off-shore wind parks, and petroleum platforms.

Description: Few studies have thus far explored the microbiomes of glass sponges (Hexactinellida). The present study seeks to elucidate the composition of the microbiota associated with the glass sponge Vazella pourtalesii and the functional strategies of the main symbionts. We combined microscopic approaches with metagenome-guided microbial genome reconstruction and amplicon community profiling towards this goal. Microscopic imaging revealed that the host and microbial cells appeared within dense biomass patches that are presumably syncytial tissue aggregates. Based on abundances in amplicon libraries and metagenomic data, SAR324 bacteria, Crenarchaeota, Patescibacteria and Nanoarchaeota were identified as abundant members of the V. pourtalesii microbiome and their genomic potentials were thus analyzed in detail. A general pattern emerged in that the V. pourtalesii symbionts had very small genome sizes in the range of 0.5-2.2 Mb and low GC contents, even below those of seawater relatives. Based on functional analyses of metagenome-assembled genomes (MAGs), we propose two major microbial strategies: the “givers”, namely Crenarchaeota and SAR324, heterotrophs and facultative anaerobes, produce and partly secrete all required amino acids and vitamins. The “takers”, Nanoarchaeota and Patescibacteria, are anaerobes with reduced genomes that tap into the microbial community for resources, e.g., lipids and DNA, likely using pili-like structures. We posit that the existence of microbial cells in sponge syncytia together with the low-oxygen conditions in the seawater environment are factors that shape the unique compositional and functional properties of the microbial community associated with V. pourtalesii . Importance: We investigated the microbial community of V. pourtalesii that forms globally unique, monospecific sponge grounds under low-oxygen conditions on the Scotian Shelf, where it plays a key role for its vulnerable ecosystem. The microbial community was found to be concentrated within biomass patches and is dominated by small cells (〈1 μm). MAG analyses showed consistently small genome sizes and low GC contents, which is unusual in comparison to known sponge symbionts. These properties as well as the (facultatively) anaerobic metabolism and a high degree of interdependence between the dominant symbionts regarding amino acid and vitamin synthesis are likely adaptations to the unique conditions within the syncytial tissue of their hexactinellid host and the low-oxygen environment.

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: Ocean ecosystems are at the forefront of the climate and biodiversity crises, yet we lack a unified approach to assess their state and inform sustainable policies. This blueprint is designed around research capabilities and cross-sectoral partnerships. We highlight priorities including integrating basin-scale observation, modelling and genomic approaches to understand Atlantic oceanography and ecosystem connectivity; improving ecosystem mapping; identifying potential tipping points in deep and open ocean ecosystems; understanding compound impacts of multiple stressors including warming, acidification and deoxygenation; enhancing spatial and temporal management and protection. We argue that these goals are best achieved through partnerships with policy-makers and community stakeholders, and promoting research groups from the South Atlantic through investment and engagement. Given the high costs of such research (€800k to €1.7M per expedition and €30–40M for a basin-scale programme), international cooperation and funding are integral to supporting science-led policies to conserve ocean ecosystems that transcend jurisdictional borders.

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.

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.