Quantifying sponge host and microbial symbiont contribution to dissolved organic matter uptake through cell separation (original) (raw)
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Single-cell visualization indicates direct role of sponge host in uptake of dissolved organic matter
Proceedings of the Royal Society B: Biological Sciences, 2019
Marine sponges are set to become more abundant in many near-future oligotrophic environments, where they play crucial roles in nutrient cycling. Of high importance is their mass turnover of dissolved organic matter (DOM), a heterogeneous mixture that constitutes the largest fraction of organic matter in the ocean and is recycled primarily by bacterial mediation. Little is known, however, about the mechanism that enables sponges to incorporate large quantities of DOM in their nutrition, unlike most other invertebrates. Here, we examine the cellular capacity for direct processing of DOM, and the fate of the processed matter, inside a dinoflagellate-hosting bioeroding sponge that is prominent on Indo-Pacific coral reefs. Integrating transmission electron microscopy with nanoscale secondary ion mass spectrometry, we track 15 N- and 13 C-enriched DOM over time at the individual cell level of an intact sponge holobiont. We show initial high enrichment in the filter-feeding cells of the sp...
Scientific Reports
Deep-sea sponges create hotspots of biodiversity and biological activity in the otherwise barren deep-sea. However, it remains elusive how sponge hosts and their microbial symbionts acquire and process food in these food-limited environments. Therefore, we traced the processing (i.e. assimilation and respiration) of 13C- and 15N-enriched dissolved organic matter (DOM) and bacteria by three dominant North Atlantic deep-sea sponges: the high microbial abundance (HMA) demosponge Geodia barretti, the low microbial abundance (LMA) demosponge Hymedesmia paupertas, and the LMA hexactinellid Vazella pourtalesii. We also assessed the assimilation of both food sources into sponge- and bacteria-specific phospholipid-derived fatty acid (PLFA) biomarkers. All sponges were capable of assimilating DOM as well as bacteria. However, processing of the two food sources differed considerably between the tested species: the DOM assimilation-to-respiration efficiency was highest for the HMA sponge, yet u...
Complex interactions between marine sponges and their symbiotic microbial communities
Limnology and Oceanography, 2011
To investigate the importance of symbiont-derived nutrition to host sponges, we coupled manipulative shading experiments with stable isotope analyses of isolated symbiont and host cell fractions. Experiments were conducted with four common reef sponges: Aplysina cauliformis, A. fulva, Neopetrosia subtriangularis, and Niphates erecta. The sponge N. erecta lacks photosymbionts, had a higher growth rate under shaded conditions, and displayed no difference in chlorophyll a (Chl a) concentrations across treatments. Isotope values suggested that this sponge obtains nutrition from particulate organic matter in the water column. In contrast, sponges hosting cyanobacterial symbionts (Aplysina spp. and Neopetrosia) had lower growth rates and lower Chl a concentrations under shaded conditions, suggesting that these hosts rely on photosymbiont nutrition. d 15 N and d 13 C values of sponge and microbial cell fractions demonstrated that, while both carbon and nitrogen are transferred from symbionts to host cells in A. cauliformis, only carbon is transferred in N. subtriangularis, and only nitrogen is transferred in A. fulva. Under shaded conditions, shifts in symbiont d 13 C values were coupled to shifts in host d 13 C values in some, but not all, host species, suggesting that the stability of these interactions varies across host species. Symbiont-derived nutrients are transferred to the cells of host sponges, and the variability observed among host species indicates that these interactions are more complex than originally hypothesized.
The ISME Journal
Sponges are the oldest known extant animal-microbe symbiosis. These ubiquitous benthic animals play an important role in marine ecosystems in the cycling of dissolved organic matter (DOM), the largest source of organic matter on Earth. The conventional view on DOM cycling through microbial processing has been challenged by the interaction between this efficient filter-feeding host and its diverse and abundant microbiome. Here we quantify, for the first time, the role of host cells and microbial symbionts in sponge heterotrophy. We combined stable isotope probing and nanoscale secondary ion mass spectrometry to compare the processing of different sources of DOM (glucose, amino acids, algal-produced) and particulate organic matter (POM) by a high-microbial abundance (HMA) and low-microbial abundance (LMA) sponge with single-cell resolution. Contrary to common notion, we found that both microbial symbionts and host choanocyte (i.e. filter) cells and were active in DOM uptake. Although ...
Limnology and Oceanography
Sponges are commonly divided into high (HMA) and low (LMA) microbial-abundance species according to the bacterial biomass in their tissue. These two groups reflect distinct aquiferous structures and feeding strategies. In the NW Mediterranean coralligenous community, HMA and LMA sponges are often packed in dense, multispecies assemblages that cover many pinnacles and overhangs. We investigated the metabolism of HMA and LMA species that cohabitate the coralligenous community by sampling in situ the inhaled and exhaled water. Sponges consumed plankton, dissolved organic carbon (DOC), and ammonium in relation to their abundance in ambient water. The plankton retention efficiency was high for all species. DOC was the main source of C for the sponge species, accounting for 90% of the examined sources. Nitrogen fluxes markedly differed between the two groups: plankton was the main source of nitrogen for LMAs that excreted dissolved organic nitrogen (DON) and ammonium. The nitrogenous waste products of LMAs were found to be the major source of nitrogen (up to 97%) for HMAs that efficiently removed DON and ammonium and excreted nitrate. The different capacity of both sponge strategies to use dissolved resources suggests a partial trophic niche separation related to HMA-LMA dichotomy as a mechanism facilitating their dense coexistence in the community. Our findings suggest that a mixed assemblage of sponges (and their associated microbes) is able to utilize the suspended particulate and dissolved material more efficiently than a single species population and may contribute to the understanding of the phenomena of the stability and diversity of dense sponge assemblages in oligotrophic habitats.
Frontiers in Marine Science
Sponges play a key role in (re)cycling of dissolved organic matter (DOM) and inorganic nutrients in coral reef ecosystems. Macroalgae and corals release different quantities of DOM and at different bioavailabilities to sponges and their microbiome. Given the current coral- to algal-dominance shift on coral reefs, we assessed the differential processing of macroalgal- and coral-DOM by three high and three low microbial abundance (HMA and LMA) encrusting sponge species. We followed the assimilation of naturally sourced 13C- and 15N-enriched macroalgal- and coral-DOM into bulk tissue and into host- versus bacteria-specific phospholipid fatty acids (PLFAs). Additionally, we compared sponge-processing of the two natural DOM sources with 13C- and 15N-enriched laboratory-made diatom-DOM. All investigated sponges utilized all DOM sources, with higher assimilation rates in LMA compared to HMA sponges. No difference was found in carbon assimilation of coral- versus macroalgal-DOM into bulk ti...