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The Scotian Shelf harbors unique aggregations of the glass sponge Vazella pourtalesii that provides an important habitat for benthic and pelagic fauna. Recent studies have shown that these sponge grounds have persisted in the face of strong inter-annual and multi-decadal variability in temperature and salinity. However, little is known of these environmental characteristics on hourly-seasonal time scales. This study presents the first hydrodynamic observations and associated (food) particle supply mechanisms for the Vazella sponge grounds, highlighting the influence of natural variability in environmental conditions on sponge growth and resilience. Near-bottom environmental conditions were characterized by high temporal resolution data collected with a benthic lander, deployed during a period of 10 months in the Sambro Bank Sponge Conservation Area. The lander was equipped with temperature and oxygen sensors, a current meter, a sediment trap and a video camera. In addition, water column profiles of temperature and salinity were collected in an array across the sponge grounds from high to lower sponge presence probability. Over the course of the lander deployment, temperature fluctuated between 8.8–12°C with an average of 10.6 ± 0.4°C. Dissolved oxygen concentration was on average 6.3 mg l–1, and near-bottom current speed was on average 0.12 m s–1, with peaks up to 0.47 m s–1. Semi-diurnal tidal currents promoted constant resuspension of particulate matter in the benthic boundary layer. Surface storm events episodically caused extremely turbid conditions on the seafloor that persisted for several days, with particles being resuspended to more than 13 m above the seabed. The carbon flux in the near-bottom sediment trap peaked during storm events and also after a spring bloom in April, when fresh phytodetritus was observed in the bottom boundary layer. While resuspension events can represent a major stressor for spo

Biogeochemical cycling of silicon (Si), largely affected by biological drivers, is pivotal to the ecological functioning of the ocean. Most knowledge regarding biological utilization of Si derives from research on phototrophic organisms circumscribed to the photic ocean (i.e., diatoms). Utilization of Si in the aphotic ocean, where heterotrophic silicifiers become relevant Si users, remains poorly investigated. Here we quantify the flux rates and stocks characterizing Si cycling across dense aggregations of the hexactinellid sponge Vazella pourtalesii established in the aphotic zone of the central Scotian Shelf, Nova Scotia, Canada. Although individual rates of silicic acid consumption were low compared to other sponge species and diatoms, the large abundance of individuals (6.5 million) over the extension of these sponge grounds (2105 km2) leads to massive annual silicic acid consumption, invested in producing their siliceous skeletons of biogenic silica. This sponge activity accumulates large biogenic silica stocks both in the living population and in the sediments. Skeletal pieces in sediment revealed that a good portion of biogenic silica deposited to the bottom after sponge death recycles as silicic acid before being permanently buried. This biogenic silica–silicic acid turnover, facilitated by an unconventional silicification pattern that favors delamination and dissolution of V. pourtalesii spicules, causes silicic acid enrichment at oceanographic dimensions in the bottom water of the central Scotian Shelf. Silicic acid efflux from the bottom sustains a feedback mechanism that fulfills sponge needs for silicic acid and facilitates the persistence of sponge aggregations in the long term.

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 aggregation

Biogeochemical cycling of silicon (Si), largely affected by biological drivers, is pivotal to the ecological functioning of the ocean. Most knowledge regarding biological utilization of Si derives from research on phototrophic organisms circumscribed to the photic ocean (i.e., diatoms). Utilization of Si in the aphotic ocean, where heterotrophic silicifiers become relevant Si users, remains poorly investigated. Here we quantify the flux rates and stocks characterizing Si cycling across dense aggregations of the hexactinellid sponge Vazella pourtalesii established in the aphotic zone of the central Scotian Shelf, Nova Scotia, Canada. Although individual rates of silicic acid consumption were low compared to other sponge species and diatoms, the large abundance of individuals (6.5 million) over the extension of these sponge grounds (2105 km2 ) leads to massive annual silicic acid consumption, invested in producing their siliceous skeletons of biogenic silica. This sponge activity accumulates large biogenic silica stocks both in the living population and in the sediments. Skeletal pieces in sediment revealed that a good portion of biogenic silica deposited to the bottom after sponge death recycles as silicic acid before being permanently buried. This biogenic silica–silicic acid turnover, facilitated by an unconventional silicification pattern that favors delamination and dissolution of V. pourtalesii spicules, causes silicic acid enrichment at oceanographic dimensions in the bottom water of the central Scotian Shelf. Silicic acid efflux from the bottom sustains a feedback mechanism that fulfills sponge needs for silicic acid and facilitates the persistence of sponge aggregations in the long term.

The biological utilization of dissolved silicon (DSi) influences ocean ecology and biogeochemistry. In the deep sea, hexactinellid sponges are major DSi consumers that remain poorly understood. Their DSi consumption departs from the Michaelis-Menten kinetics of shallow-water demosponges and appears particularly maladapted to incorporating DSi from the modest concentrations typical of the modern ocean. Why did sponges not adapt to the shrinking DSi availability that followed diatom expansion some 100 to 65 million years ago? We propose that sponges incorporate DSi combining passive (aquaglyceroporins) and active (ArsB) transporters, while only active transporters (SITs) operate in diatoms and choanoflagellates. Evolution of greater silicon transport efficiency appears constrained by the additional role of aquaglyceroporins in transporting essential metalloids other than silicon. We discuss the possibility that lower energy costs may have driven replacement of ancestral SITs by less efficient aquaglyceroporins, and discuss the functional implications of conservation of aquaglyceroporin-mediated DSi utilization in vertebrates.