Sponges With Microbial Symbionts Transform Dissolved Organic Matter and Take Up Organohalides

Lauren K Olinger,Steven E Mcmurray,Wendy K Strangman,Joseph R Pawlik

doi:10.3389/fmars.2021.665789

Lauren K Olinger, Steven E Mcmurray + Show 2 more

Open Access

https://doi.org/10.3389/fmars.2021.665789

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Abstract

Seawater dissolved organic matter (DOM) is a large reservoir of carbon composed of a complex and poorly characterized mixture of molecules. Sponges have long been known to consume dissolved organic carbon (DOC) from this mixture, but the role of microbial sponge symbionts in this process is complex, and the molecules involved remain largely unknown. In order to better understand how sponge processing changes seawater DOM, we used untargeted metabolomics to characterize DOM in samples of incurrent and excurrent seawater taken from sponges on the fore-reef off Carrie Bow Cay, Belize, over 2 years. We collected samples from three sponge species each with either high or low microbial abundance (HMA, LMA) to explore the relationship between symbiont abundance and DOM alterations. Analyses revealed that sponges took up metabolites and changed the composition of seawater DOM, but only for the three HMA species, and none of the LMA species, implicating microbial symbionts in this uptake. Using a new mass spectra classification tool, we found that putative compositions of features depleted in the excurrent samples of HMA sponges were similar in both years and were dominated by organic acids and derivatives (74%) and organic nitrogen compounds (19%). Interestingly, HMA sponges also took up halogenated compounds (containing chlorine or bromine), providing evidence of a previously unknown mechanism of halide cycling. The metabolites taken up by HMA sponges may be used as a food source or as building blocks of chemical defenses, selective advantages that may have guided the evolution of microbial symbioses in sponges.

Highlights

Sponges are important members of most aquatic habitats, ranging from the tropics to the polar seas, and from the intertidal zone to the deep-sea (Wörheide et al, 2005)
While low microbial abundance (LMA) sponges made negligible changes to seawater dissolved organic matter (DOM), the DOM profile of incurrent and excurrent (In/Ex) samples from high microbial abundance (HMA) sponges revealed considerable and uniform In/Ex differences driven by mass features that were depleted by the sponge
Whether dissolved organic carbon (DOC) uptake is common across HMA and LMA sponge species has been the subject of conflicting studies

Summary

Introduction

Sponges are important members of most aquatic habitats, ranging from the tropics to the polar seas, and from the intertidal zone to the deep-sea (Wörheide et al, 2005). 2000 and 2012 (McMurray et al, 2015) Massive sponges such as X. muta are efficient filter feeders capable of overturning a 30 m water column in as little as 2.3 days (McMurray et al, 2014). As they pump seawater through their aquiferous system, sponges assimilate dietary carbon in forms ranging in size from particulate to dissolved. Efforts to quantify and isotopically trace the DOC taken up by sponges have revealed the biogeochemical importance of this group and have inspired novel hypotheses, such as the “sponge loop,” which proposes that sponges retain carbon on coral reefs by converting carbon from DOC to forms such as particulate detritus or biomass that are accessible to higher trophic levels (de Goeij et al, 2013; McMurray et al, 2018)

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