Processing of Naturally Sourced Macroalgal- and Coral-Dissolved Organic Matter (DOM) by High and Low Microbial Abundance Encrusting Sponges

Sara Campana,Jorien Schoorl,Anna De Kluijver,Meggie Hudspith,Celine Demey,Jasper M De Goeij,Benjamin Mueller,David Lankes,Marcel T J Van Der Meer,Samira Absalah

doi:10.3389/fmars.2021.640583

Abstract

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 tissue and host- versus bacteria-specific PLFAs, but macroalgal nitrogen was assimilated into bulk tissue up to eight times faster compared to the other sources, indicating its higher bioavailability to the sponges. Additionally, LMA sponges released significantly more inorganic nitrogen after feeding on macroalgal-DOM. Therefore, we hypothesize that, depending on the abundance and composition of the sponge community, sponges could catalyze reef eutrophication through increased turnover of nitrogen under coral-to-algal regime shifts.

Highlights

Coral reefs are marine ecosystems thriving in oligotrophic waters
As a first step to assess the role of sponges in the cycling of different naturally available dissolved organic matter (DOM) sources, we studied the differential processing of macroalgal- and coralDOM by low microbial abundance (LMA) and high microbial abundance (HMA) encrusting sponge holobionts
This study shows the differential processing of two natural DOM sources derived from macroalgae and corals by six Caribbean encrusting sponge species with different microbial abundances

Summary

Introduction

Coral reefs are marine ecosystems thriving in oligotrophic waters. Despite being characterized by low nutrient concentrations, these ecosystems are highly productive and hotspots of biodiversity (Hatcher, 1990; Knowlton et al, 2010). The processing of DOM by bacterioplankton and its subsequent recycling through the microbial loop is well established (Azam et al, 1983; Haas et al, 2011; Nelson and Carlson, 2012), but in recent years, sponges have been shown to play a major role in DOM recycling on coral reefs via the so-called “sponge loop” pathway (de Goeij et al, 2013). Conversion of DOM into detrital POM is mainly observed in encrusting sponge species (Alexander et al, 2014) that dominate the benthos of the cryptic habitats of reefs (e.g., overhangs, crevices, cavities), and appear on exposed surfaces (Richter et al, 2001; Scheffers et al, 2005). Upward growing, non-encrusting sponges (e.g., massive, branching), which predominantly appear on exposed surfaces, are hypothesized to cycle DOM through a predatory sponge loop pathway, by investing more resources in net growth and being preyed upon by spongivores (McMurray et al, 2018; Pawlik and McMurray, 2020)

Methods

Results

Conclusion