Nutrient fluxes, oxygen consumption and fatty acid composition from deep-water demo- and hexactinellid sponges from New Zealand

Sponges are an important component of deep-water ecosystems enhancing eukaryotic biodiversity by hosting diverse endo- and epibiota and providing three dimensional habitats for benthic invertebrates and fishes. As holobionts they are important hosts of microorganisms which are involved in carbon and nitrogen cycling. While increasing exploration of deep-water habitats results in new sponge species being discovered, little is known about their physiology and role in nutrient fluxes. Around New Zealand (Southwest Pacific), the sponge biodiversity is particularly high, and we selected six deep-sea sponge genera (Saccocalyx, Suberites, Tedania, Halichondria/Dendoricella, Lissodendoryx) and a member of the Sceptrulophora order for in-situ and ex-situ experiments.

We investigated the biochemical composition of the sponges, measured oxygen consumption and inorganic nutrient fluxes, as well as bacterial and phospholipid-derived fatty acid (PLFA) compositions. Our aim was to assess differences in fluxes and fatty acid composition among sponges and linking their bacterial communities to nitrogen cycling processes.

All sponges excreted nitrite and ammonia. Nitrate and phosphate excretion were independent of phylum affiliation (Demospongiae, Hexactinellida). Nitrate was excreted by Halichondria/Dendoricella and Lissodendoryx, whereas Suberites, Tedania, and Sceptrulophora consumed it. Phosphate was excreted by Sceptrulophora and Halichondria/Dendoricella and consumed by all other sponges. Oxygen consumption rates ranged from 0.17 to 3.56 ± 0.60 mmol O₂ g C^-1 d⁻¹.

The PLFA composition was very sponge-genera dependent and consisted mostly of long-chain fatty acids. Most PLFAs were sponge-specific, followed by bacteria-specific PLFAs, and others.

All sponges, except for Suberites, were low-microbial abundance (LMA) sponges whose bacterial community composition was dominated by Proteobacteria, Bacteroidota, Planctomycetota, and Nitrospinota. Suberites consisted of high-microbial abundance (HMA) sponges with Proteobacteria, Chloroflexota, Acidobacteriota, and Actinobacteriota as dominant bacteria.

Based on the inorganic nitrogen flux measurements, we identified three types of nitrogen cycling in the sponges: In type 1, sponges (Dendoricella spp. indet., Lissodendoryx) respired aerobically and ammonificated organic matter (OM) to ammonium, fixed N₂ to ammonium, and nitrified aerobically heterotrophically produced ammonium to nitrate and nitrite. In type 2, sponges (Halichondria sp., Sceptrulophora, Suberites, Tedania) respired OM aerobically and ammonificated it to ammonium. They also reduced nitrate anaerobically to ammonium via dissimilatory nitrate reduction to ammonium. In type 3, ammonium was microbially nitrified to nitrite and afterwards to nitrate presumably by ammonium-oxidizing Bacteria and/or Archaea.