Abstract
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 all DOM sources were assimilated by both sponges, higher microbial biomass in the HMA sponge corresponded to an increased capacity to process a greater variety of dissolved compounds. Nevertheless, in situ feeding data demonstrated that DOM was the primary carbon source for both the LMA and HMA sponge, accounting for ~90% of their heterotrophic diets. Microbes accounted for the majority (65–87%) of DOM assimilated by the HMA sponge (and ~60% of its total heterotrophic diet) but <5% in the LMA sponge. We propose that the evolutionary success of sponges is due to their different strategies to exploit the vast reservoir of DOM in the ocean.
Highlights
As the oldest extant animal phyla, sponges have thrived on Earth for more than 600 million years
stable isotope probing (SIP) experiments showed that all four food sources were assimilated into the bulk tissue of both the high-microbial abundance (HMA) sponge A. aerophoba and low-microbial abundance (LMA) sponge D. avara, but they exhibited significant differences in assimilation rates (Fig. 2a–d)
Microbial contributions to total sponge heterotrophic diet are higher in the HMA sponge Despite significant differences in dissolved organic matter (DOM) uptake rates between the two sponges in the isotope tracer experiments, in which food was supplied in excess of natural concentrations (Fig. 2a–d), we found that the natural diets of the two sponges were more similar when measured in situ under natural concentrations (Fig. 5)
Summary
Specimens of Aplysina aerophoba and Dysidea avara (n = 20) were collected by SCUBA from the coast of Girona, Spain (42° 06′ 55′′ N, 3° 10′ 8′′ E) at depths of 3–15 m during April and May 2017. Each sponge individual was divided into five fragments of a similar size, each with a single fully functional osculum, and attached to PVC plates. Sponges were acclimated for 5 days and only healthy, actively pumping individuals were used in experiments. Stable isotope pulse-chase experiments were conducted to test for the assimilation of three dissolved (13C-glucose, 13C- and 15N-amino acids, 13C- and 15N-algal DOM) and one particulate food source (13C- and 15N-labeled bacteria). Details of the preparation of the four food sources are described in the Supplementary Methods. Food sources were added to individual 6 L aquaria
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