Description: Time-series studies of arctic marine ecosystems are rare. This is not surprising since polar regions are largely only accessible by means of expensive modern infrastructure and instrumentation. In 1999, the Alfred Wegener Institute, Helmholtz-Centre for Polar and Marine Research (AWI) established the LTER (Long-Term Ecological Research) observatory HAUSGARTEN crossing the Fram Strait at about 79° N. Multidisciplinary investigations covering all parts of the open-ocean ecosystem are carried out at a total of 21 permanent sampling sites in water depths ranging between 250 and 5500 m. From the outset, repeated sampling in the water column and at the deep seafloor during regular expeditions in summer months was complemented by continuous year-round sampling and sensing using autonomous instruments in anchored devices (i.e., moorings and free-falling systems). The central HAUSGARTEN station at 2500 m water depth in the eastern Fram Strait serves as an experimental area for unique biological in situ experiments at the seafloor, simulating various scenarios in changing environmental settings. Long-term ecological research at the HAUSGARTEN observatory revealed a number of interesting temporal trends in numerous biological variables from the pelagic system to the deep seafloor. Contrary to common intuition, the entire ecosystem responded exceptionally fast to environmental changes in the upper water column. Major variations were associated with a Warm-Water-Anomaly evident in surface waters in eastern parts of the Fram Strait between 2005 and 2008. However, even after 15 years of intense time-series work at HAUSGARTEN, we cannot yet predict with complete certainty whether these trends indicate lasting alterations due to anthropologically-induced global environmental changes of the system, or whether they reflect natural variability on multiyear time-scales, for example, in relation to decadal oscillatory atmospheric processes.

Description: Most animals, including sponges (Porifera), have species-specific microbiomes. Which genetic or environmental factors play major roles structuring the microbial community at the intraspecific level in sponges is, however, largely unknown. In this study, we tested whether geographic location or genetic structure of conspecific sponges influences their microbial assembly. For that, we used three sponge species with different rates of gene flow, and collected samples along their entire distribution range (two from the Mediterranean and one from the Southern Ocean) yielding a total of 393 samples. These three sponge species have been previously analysed by microsatellites or single nucleotide polymorphisms, and here we investigate their microbiomes by amplicon sequencing of the microbial 16S rRNA gene. The sponge Petrosia ficiformis, with highly isolated populations (low gene flow), showed a stronger influence of the host genetic distance on the microbial composition than the spatial distance. Host-specificity was therefore detected at the genotypic level, with individuals belonging to the same host genetic cluster harbouring more similar microbiomes than distant ones. On the contrary, the microbiome of Ircinia fasciculata and Dendrilla antarctica - both with weak population structure (high gene flow) - seemed influenced by location rather than by host genetic distance. Our results suggest that in sponge species with high population structure, the host genetic cluster influence the microbial community more than the geographic location.

Description: Marine sponges are known for their complex and stable microbiomes. However, the lack of a gnotobiotic sponge-model and experimental methods to manipulate both the host and the microbial symbionts currently limit our mechanistic understanding of sponge-microbial symbioses. We have used the North Atlantic sponge species Halichondria panicea to evaluate the use of antibiotics to generate gnotobiotic sponges. We further asked whether the microbiome can be reestablished via recolonization with the natural microbiome. Experiments were performed in marine gnotobiotic facilities equipped with a custom-made, sterile, flow-through aquarium system. Bacterial abundance dynamics were monitored qualitatively and quantitatively by 16 S rRNA gene amplicon sequencing and qPCR, respectively. Antibiotics induced dysbiosis by favouring an increase of opportunistic, antibiotic-resistant bacteria, resulting in more complex, but less specific bacteria-bacteria interactions than in untreated sponges. The abundance of the dominant symbiont, Candidatus Halichondribacter symbioticus, remained overall unchanged, reflecting its obligately symbiotic nature. Recolonization with the natural microbiome could not reverse antibiotic-induced dysbiosis. However, single bacterial taxa that were transferred, successfully recolonized the sponge and affected bacteria-bacteria interactions. By experimentally manipulating microbiome composition, we could show the stability of a sponge-symbiont clade despite microbiome dysbiosis. This study contributes to understanding both host-bacteria and bacteria-bacteria interactions in the sponge holobiont.

Description: The deep-sea is vast, remote, and largely underexplored. However, methodological advances in environmental DNA (eDNA) surveys could aid in the exploration efforts, such as using sponges as natural eDNA filters for studying fish biodiversity. In this study, we analyzed the eDNA from 116 sponge tissue samples and compared these to 18 water eDNA samples and visual surveys obtained on an Arctic seamount. Across survey methods, we revealed approximately 30% of the species presumed to inhabit this area and 11 fish species were detected via sponge derived eDNA alone. These included commercially important fish such as the Greenland halibut and Atlantic mackerel. Fish eDNA detection was highly variable across sponge samples. Highest detection rates were found in sponges with low microbial activity such as those from the class Hexactinellida. The different survey methods also detected alternate fish communities, highlighted by only one species overlap between the visual surveys and the sponge eDNA samples. Therefore, we conclude that sponge eDNA can be a useful tool for surveying deep-sea demersal fish communities and it synergises with visual surveys improving overall biodiversity assessments. Datasets such as this can form comprehensive baselines on fish biodiversity across seamounts, which in turn can inform marine management and conservation practices in the regions where such surveys are undertaken.

Description: Highlights: • Fan-shaped sponges display panmixia at three locations in the Cantabrian Sea. • Subtle sponge population genetic and pronounced microbial differences were observed between a canyon and bank (〈100km apart). • Lagrangian modelling reveals variable inter-annual connectivity via ocean currents between the sampling regions. • Interdisciplinary approaches can help to improve understanding about connectivity in the deep-sea. Abstract: Connectivity is a fundamental process driving the persistence of marine populations and their adaptation potential in response to environmental change. In this study, we analysed the population genetics of two morphologically highly similar deep-sea sponge clades (Phakellia hirondellei and the ‘Topsentia-and-Petromica’ clade, (hereafter referred to as ‘TaP clade’)) at three locations in the Cantabrian Sea and simultaneously assessed the corresponding host microbiome by 16S rRNA gene sequencing. A virtual particle tracking approach (Lagrangian modelling) was applied to assess oceanographic connectivity in the study area. We observed overall genetic uniformity for both sponge clades. Notably, subtle genetic differences were observed for sponges of the TaP clade and also their microbiomes between a canyon and bank location, 〈 100 km apart and with the same depth range. The Lagrangian model output suggests a strong retention of larvae in the study area with variable inter-annual connectivity via currents between the three sampling regions. We conclude that geologic features (canyons) and the prevailing ocean currents may dictate sponge holobiont connectivity and that differentiation can emerge even on small spatial scales.

Description: Sponges possess exceptionally diverse associated microbial communities and play a major role in (re)cycling of dissolved organic matter (DOM) in marine ecosystems. Linking sponge-associated community structure with DOM utilization is essential to understand host-microbe interactions in the uptake, processing, and exchange of resources. We coupled, for the first time, DNA-stable isotope probing (DNA-SIP) with 16S rRNA amplicon sequencing in a sponge holobiont to identify which symbiotic bacterial taxa are metabolically active in DOM uptake. Parallel incubation experiments with the sponge Plakortis angulospiculatus were amended with equimolar quantities of unlabelled (C-12) and labelled (C-13) DOM. Seven bacterial amplicon sequence variants (ASVs), belonging to the phyla PAUC34f, Proteobacteria, Poribacteria, Nitrospirae, and Chloroflexi, were identified as the first active consumers of DOM. Our results support the predictions that PAUC34f, Poribacteria, and Chloroflexi are capable of organic matter degradation through heterotrophic carbon metabolism, while Nitrospirae may have a potential mixotrophic metabolism. We present a new analytical application of DNA-SIP to detect substrate incorporation into a marine holobiont with a complex associated bacterial community and provide new experimental evidence that links the identity of diverse sponge-associated bacteria to the consumption of DOM.

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: The collection of zooplankton swimmers and sinkers in time-series sediment traps provides unique insight into year-round and interannual trends in zooplankton population dynamics. These samples are particularly valuable in remote and difficult to access areas such as the Arctic Ocean, where samples from the ice-covered season are rare. In the present study, we investigated zooplankton composition based on swimmers and sinkers collected by sediment traps at water depths of 180–280, 800–1320, and 2320–2550 m, over a period of 16 yr (2000–2016) at the Long-Term Ecological Research observatory HAUSGARTEN located in the eastern Fram Strait (79°N, 4°E). The time-series data showed seasonal and interannual trends within the dominant zooplankton groups including copepoda, foraminifera, ostracoda, amphipoda, pteropoda, and chaetognatha. Amphipoda and copepoda dominated the abundance of swimmers while pteropoda and foraminifera were the most important sinkers. Although the seasonal occurrence of these groups was relatively consistent between years, there were notable interannual variations in abundance, suggesting the influence of various environmental conditions such as sea-ice dynamic and lateral advection of water masses, for example, meltwater and Atlantic water. Statistical analyses revealed a correlation between the Arctic dipole climatic index and sea-ice dynamics (i.e., ice coverage and concentration), as well as the importance of the distance from the ice edge on swimmer composition patterns and carbon export.

Description: Abundant mineral resources in the deep sea are prospected for mining for the global metal market. Seafloor massive sulphide (SMS) deposits along the Mid-Atlantic Ridge are one of the potential sources for these metals. The extraction of SMS deposits will expose adjacent marine ecosystems to suspended particle plumes charged with elevated concentrations of heavy metals and other potentially toxic compounds. Up to date there is no information about the impact of mining activities on deep-sea benthic ecosystems such as abundant deep-sea sponge grounds in the North Atlantic Ocean. Sponge grounds play a major role in benthic-pelagic coupling and represent an important habitat for a diversity of vertebrates, invertebrates and microorganisms. To simulate the effects of mining plumes on benthic life in the deep sea, we exposed Geodia barretti, a dominant sponge species in the North Atlantic Ocean, and an associated brittle star species from the genus Ophiura spp. to a field-relevant concentration of 30 mg L−1 suspended particles of crushed SMS deposits. Three weeks of exposure to suspended particles of crushed SMS resulted in a tenfold higher rate of tissue necrosis in sponges. All brittle stars in the experiment perished within ten days of exposure. SMS particles were evidently accumulated in the sponge's mesohyl and concentrations of iron and copper were 10 times elevated in SMS exposed individuals. Oxygen consumption and clearance rates were significantly retarded after the exposure to SMS particles, hampering the physiological performance of G. barretti. These adverse effects of crushed SMS deposits on G. barretti and its associated brittle star species potentially cascade in disruptions of benthic-pelagic coupling processes in the deep sea. More elaborate studies are advisable to identify threshold levels, management concepts and mitigation measures to minimize the impact of deep-sea mining plumes on benthic life.