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 of13C- and15Nenriched DOM into sponge cells and microbial symbionts of the encrusting Caribbean spongesHaliclona vansoestiandScopalina 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.
Highlights
Symbioses are widespread in nature and are defined in the broadest sense as intimate and enduring associations between different organisms, which lie on a continuum spanning mutualistic to parasiticMar Ecol Prog Ser 670: 1–13, 2021 interactions (Paracer & Ahmadjian 2000)
Stable isotopic enrichment of bulk sponge tissue after the pulse period translated to dissolved organic matter (DOM) incorporation rates of 1.11 ± 0.04 μmol CDOM mmol Csponge−1 h−1 and 1.15 ± 0.06 μmol NDOM mmol Nsponge−1 h−1 for H. vansoesti, and 0.73 ± 0.07 μmol CDOM mmol Csponge−1 h−1 and 0.65 ± 0.04 μmol NDOM mmol Nsponge−1 h−1 for S. ruetzleri
Studies investigating the relative contribution of sponge host and microbiome to DOM uptake and the subsequent exchange of nutrients, are limited (Achlatis et al 2019, Rix et al 2020, Hudspith et al 2021)
Summary
Symbioses are widespread in nature and are defined in the broadest sense as intimate and enduring associations between different organisms, which lie on a continuum spanning mutualistic to parasitic. Quantifying the relative contribution of sponge cells and microbial symbionts to DOM assimilation remains challenging, and to date has only been achieved in 2 Mediterranean species with massive growth forms (Rix et al 2020). Host versus symbiont contribution to heterotrophy was suggested to be driven by their relative biomass in the holobiont rather than single-cell differences in assimilation rates Whether this applies to sponges with different growth forms (e.g. encrusting, massive) and across different ecosystems, such as tropical coral reefs and deep-sea sponge grounds, is not known. We investigate the relative contribution of sponge cells and microbial symbionts to DOM assimilation and the subsequent translocation of nutrients by combining stable isotope probing (SIP) with the separation of host cell and symbiont fractions.
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