Quantifying sponge host and microbial symbiont contribution to dissolved organic matter uptake through cell separation

Abstract

Sponge−microbe symbioses underpin the ecological success of sponges in many aquatic benthic ecosystems worldwide. These symbioses are often described as mutually beneficial, but identifying positive symbiotic interactions and quantifying the contribution of partners to physiological processes is challenging. For example, our understanding of the relative contribution of sponge cells and their microbial symbionts to the uptake and exchange of dissolved organic matter (DOM) - a major component of sponge diet - is limited. Here, we combined host− symbiont cell separation with pulse-chase isotopic labelling in order to trace the uptake of 13C- and 15N-enriched DOM into sponge cells and microbial symbionts of the encrusting Caribbean sponges Haliclona vansoesti and Scopalina ruetzleri, which are low microbial abundance (LMA) species. Sponge cells were responsible for >99% of DOM assimilation during the pulse-chase experiment for both sponge species, while the contribution of symbiotic microbes to total DOM uptake was negligible (<1%). Nitrogen derived from DOM was translocated from sponge cells to microbial cells over time, indicating processing of host nitrogenous wastes by microbial endosymbionts. Thus, host cells drive DOM uptake in these species, while microbial symbionts may aid in the recycling of host-waste products. Our findings highlight the ability of sponges to derive nutrition by internalizing dissolved compounds from their environment and retaining nutrients via host−microbe interactions.