A Deep-Sea Sponge Loop? Sponges Transfer Dissolved and Particulate Organic Carbon and Nitrogen to Associated Fauna

Cold-water coral reefs and sponge grounds are deep-sea biological hotspots, equivalent to shallow-water tropical coral reefs. In tropical ecosystems, biodiversity and productivity are maintained through efficient recycling pathways, such as the sponge loop. In this pathway, encrusting sponges recycle dissolved organic matter (DOM) into particulate detritus. Subsequently, the sponge-produced detritus serves as a food source for other organisms on the reef. Alternatively, the DOM stored in massive sponges was recently hypothesized to be transferred to higher trophic levels through predation of these sponges, instead of detritus production. However, for deep-sea sponges, the existence of all prerequisite, consecutive steps of the sponge loop have not yet been established. Here, we tested whether cold-water deep-sea sponges, similar to their tropical shallow-water counterparts, take up DOM and transfer assimilated DOM to associated fauna via either detritus production or predation. We traced the fate of 13carbon (C)- and 15nitrogen (N)-enriched DOM and particulate organic matter (POM) in time using a pulse-chase approach. During the 24-h pulse, the uptake of 13C/15N-enriched DOM and POM by two deep-sea sponge species, the massive species Geodia barretti and the encrusting species Hymedesmia sp., was assessed. During the subsequent 9-day chase in label-free seawater, we investigated the transfer of the consumed food by sponges into brittle stars via two possible scenarios: (1) the production and subsequent consumption of detrital waste or (2) direct feeding on sponge tissue. We found that particulate detritus released by both sponge species contained C from the previously consumed tracer DOM and POM, and, after 9-day exposure to the labeled sponges and detritus, enrichment of 13C and 15N was also detected in the tissue of the brittle stars. These results therefore provide the first evidence of all consecutive steps of a sponge loop pathway via deep-sea sponges. We cannot distinguish at present whether the deep-sea sponge loop is acting through a detrital or predatory pathway, but conclude that both scenarios are feasible. We conclude that sponges could play an important role in the recycling of DOM in the many deep-sea ecosystems where they are abundant, although in situ measurements are needed to confirm this hypothesis.publishedVersio

Nocturnal dissolved organic matter release by turf algae and its role in the microbialization of reefs

The increased release of dissolved organic matter (DOM) by algae has been associated with the fast but inefficient growth of opportunistic microbial pathogens and the ongoing degradation of coral reefs. Turf algae (consortia of microalgae and macroalgae commonly including cyanobacteria) dominate benthic communities on many reefs worldwide. Opposite to other reef algae that predominantly release DOM during the day, turf algae containing cyanobacteria may additionally release large amounts of DOM at night. However, this night-DOM release and its potential contribution to the microbialization of reefs remains to be investigated. We first tested the occurrence of hypoxic conditions at the turf algae-water interface, as a lack of oxygen will facilitate the production and release of fermentation intermediates as night-time DOM. Second, the dissolved organic carbon (DOC) release by turf algae was quantified during day time and nighttime, and the quality of day and night exudates as food for bacterioplankton was tested. Finally, DOC release rates of turf algae were combined with estimates of DOC release based on benthic community composition in 1973 and 2013 to explore how changes in benthic community composition affected the contribution of night-DOC to the reef-wide DOC production. A rapid shift from supersaturated to hypoxic conditions at the turf algae-water interface occurred immediately after the onset of darkness, resulting in night-DOC release rates similar to those during daytime. Bioassays revealed major differences in the quality between day and night exudates: Night-DOC was utilized by bacterioplankton two times faster than day-DOC, but yielded a four times lower growth efficiency. Changes in benthic community composition were estimated to have resulted in a doubling of DOC release since 1973, due to an increasing abundance of benthic cyanobacterial mats (BCMs), with night-DOC release by BCMs and turf algae accounting for >50% of the total release over a diurnal cycle. Night-DOC released by BCMs and turf algae is likely an important driver in the microbialization of reefs by stimulating microbial respiration at the expense of energy and nutrient transfer to higher trophic levels via the microbial loop, thereby threatening the productivity and biodiversity of these unique ecosystems. Read the free Plain Language Summary for this article on the Journal blog