A Microbial Nitrogen Engine Modulated by Bacteriosyncytia in Hexactinellid Sponges: Ecological Implications for Deep-Sea Communities

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.

Cooperation between passive and active silicon transporters clarifies the ecophysiology and evolution of biosilicification in sponges

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.

Discovery of the sponge-associated caridean genus Paralebbeus in New Zealand and southeastern Australia: P. pegasus sp. nov. (Crustacea: Decapoda: Thoridae)

Deepwater sampling in New Zealand and southern Australian waters over the past two decades has significantly improved knowledge of all invertebrate groups, including decapod crustaceans. Thorid shrimps of the genus, Paralebbeus Bruce & Chace, 1986 are associated with deepwater hexactinellid sponges, with four species known to date from scattered localities in the southwestern Indian Ocean, northwestern Australia, Southeast Asia and the northwestern Pacific including Japan. Paralebbeus pegasus sp. nov. is described from New Zealand and southeastern Australia, representing the first record of the genus from the temperate southwestern Pacific. The new species of Paralebbeus is unique in the genus for having meral spines on pereopods 3–5. A key to the species of Paralebbeus and global distribution map are provided.

Inventory of the eastern Bering Sea sponge fauna, geographic range extensions and description of Antho ridgwayi sp. nov.

A total of 493 sponges were collected with a bottom trawl during annual groundfish stock assessment surveys in the eastern Bering Sea in 2013, 2015, and 2016 to build an inventory of species in this largely unexplored region. We report here principally on the demosponge fauna collected during those surveys because identifications of hexactinellids are incomplete. We identified 42 unique demosponge taxa from the collection including geographical range extensions for 30 species; seven are new records for the Pacific Ocean. The collection also included three species new to science; two have been previously described (Plicatellopsis borealis Lehnert & Stone 2017, Spongosorites beringensis Lehnert & Stone 2017) and Antho ridgwayi sp. nov. described here. The new species differed from all northern hemisphere congeners in the complements and sizes of spicules. We document that the region is more species rich than previously suspected, particularly the continental slope where the majority of hexactinellid sponges are located.

Partial Mitochondrial Genome Sequences of Two Abyssal Sponges (Porifera: Hexactinellida), Bathydorus laniger and Docosaccus maculatus

ABSTRACT We announce the nearly complete mitochondrial genome sequences of two hexactinellid sponges, Bathydorus laniger and Docosaccus maculatus. A contiguous region of over 15,000 bp was sequenced from each genome. An uncommon structural element was identified as a series of repetitive elements with sequences matching cob in the genome of D. maculatus.

New hexactinellid sponges from deep Mediterranean canyons

During the exploration of the NW Mediterranean deep-sea canyons (MedSeaCan and CorSeaCan cruises), several hexactinellid sponges were observed and collected by ROV and manned submersible. Two of them appeared to be new species of Farrea and Tretodictyum. The genus Farrea had so far been reported with doubt from the Mediterranean and was listed as "taxa inquirenda" for two undescribed species. We here provide a proper description for the specimens encountered and sampled. The genus Tretodictyum had been recorded several times in the Mediterranean and in the near Atlantic as T. tubulosum Schulze, 1866, again with doubt, since the type locality is the Japan Sea. We here confirm that the Mediterranean specimens are a distinct new species which we describe. We also provide18S rDNA sequences of the two new species and include them in a phylogenetic tree of related hexactinellids.