Nitrogen Biogeochemistry in the Caribbean Sponge, Xestospongia muta: A Source or Sink of Dissolved Inorganic Nitrogen?

Abstract

BackgroundSponges have long been known to be ecologically important members of the benthic fauna on coral reefs. Recently, it has been shown that sponges are also important contributors to the nitrogen biogeochemistry of coral reefs. The studies that have been done show that most sponges are net sources of dissolved inorganic nitrogen (DIN; NH4 + and NO3 −) and that nitrification, mediated by their symbiotic prokaryotes, is the primary process involved in supplying DIN to adjacent reefs.Methodology/Principal FindingsA natural experiment was conducted with the Caribbean sponge Xestospongia muta from three different locations (Florida Keys, USA; Lee Stocking Island, Bahamas and Little Cayman, Cayman Islands). The DIN fluxes of sponges were studied using nutrient analysis, stable isotope ratios, and isotope tracer experiments. Results showed that the fluxes of DIN were variable between locations and that X. muta can be either a source or sink of DIN. Stable isotope values of sponge and symbiotic bacterial fractions indicate that the prokaryotic community is capable of taking up both NH4 + and NO3 − while the differences in δ 15N between the sponge and bacterial fractions from the NH4 + tracer experiment suggest that there is translocation of labeled N from the symbiotic bacteria to the host.Conclusions/SignificanceNitrogen cycling in X. muta appears to be more complex than previous studies have shown and our results suggest that anaerobic processes such as denitrification or anammox occur in these sponges in addition to aerobic nitrification. Furthermore, the metabolism of this sponge and its prokaryotic symbionts may have a significant impact on the nitrogen biogeochemistry on Caribbean coral reefs by releasing large amounts of DIN, including higher NH4 + concentrations that previously reported.

Trait-mediated ecosystem impacts: how morphology and size affect pumping rates of the Caribbean giant barrel sponge

“…; calculated from data in Fiore et al 2013, their Table 1) is double the mean pumping rate found in the present study. This is the first study since the work of Reiswig (1974) to directly investigate the relationship between spongocoel morphology and excurrent flow.…”

“…For example, Baikalospongia bacillifera and B. intermedia from Lake Baikal, Russia, were found to re move 1870 mg C d −1 m −2 of prokaryotic picoplankton, resulting in a picoplankton-depleted layer of water within 1 m of the benthos, but were a source of 750 mg C d −1 m −2 of eukaryotic picoplankton (Pile et al 1997). Sponges are also important in nitrogen cycling and release large amounts of dissolved inorganic nitrogen that may influence levels of primary production on coral reefs (Southwell et al 2008, Fiore et al 2013. Mass mortality of the Florida Bay sponge community resulted in an increase in the average water column turnover rate by as much as 12 d for some regions of the Bay and could account for the increased algal blooms reported there (Peterson et al 2006).…”

“…The large range of excurrent profiles reported here emphasizes the need for such measurements to accurately estimate sponge pumping rates. For example, the mean pumping rate for 12 specimens of X. muta on Conch Reef, Florida, and Lee Stocking Island, Bahamas, estimated by Fiore et al (2013) by measuring the speed of dye fronts at the osculum centerline and assuming plug flow (0.12 ± 0.13 l s −1 l −1…”

“…They efficiently process large volumes of water and thereby play important roles in benthic−pelagic coupling (Pile et al 1997, Bak et al 1998, organic matter cycling (Reiswig 1974, Yahel et al 2003 and nutrient element cycling (Southwell et al 2008, Fiore et al 2013. By modifying the biotic and abiotic properties ABSTRACT: Sponges are a dominant component of Caribbean coral reef suspension-feeding communities.…”

Draft Genomes Shed Light on the Dual Bacterial Symbiosis that Dominates the Microbiome of the Coral Reef Sponge Amphimedon queenslandica

“…Their ecosystem engineering roles are enabled by diverse communities of symbiotic prokaryotes that can account for up to 40% of the sponge body volume (Taylor et al, 2007a,b;Webster et al, 2010;Hentschel et al, 2012). The symbionts extend the metabolic capabilities of the host by mediating processes, such as photosynthesis (Wilkinson, 1983;Arillo et al, 1993;Steindler et al, 2002), carbon (De Goeij et al, 2008a,b;de Goeij et al, 2013), nitrogen (Wilkinson and Fay, 2004;Mohamed et al, 2008;Southwell et al, 2008a;Hoffmann et al, 2009;Schläppy et al, 2010;Fiore et al, 2013), methane (Vacelet et al, 1995), sulfur (Hoffmann et al, 2005), and phosphorus (Sabarathnam et al, 2010;Zhang et al, 2015b) cycling. Metagenomic and transcriptomic studies of sponge microbiomes have provided independent molecular evidence of the contribution of symbiotic bacteria, in particular, to biogeochemical and nutrient cycling Fiore et al, 2015;Rua et al, 2015), underscoring the significance of the holobiont perspective in understanding ecological roles of animal hosts in marine ecosystems.…”