Cell Turnover and Detritus Production in Marine Sponges from Tropical and Temperate Benthic Ecosystems

Abstract

This study describes in vivo cell turnover (the balance between cell proliferation and cell loss) in eight marine sponge species from tropical coral reef, mangrove and temperate Mediterranean reef ecosystems. Cell proliferation was determined through the incorporation of 5-bromo-2′-deoxyuridine (BrdU) and measuring the percentage of BrdU-positive cells after 6 h of continuous labeling (10 h for Chondrosia reniformis). Apoptosis was identified using an antibody against active caspase-3. Cell loss through shedding was studied quantitatively by collecting and weighing sponge-expelled detritus and qualitatively by light microscopy of sponge tissue and detritus. All species investigated displayed substantial cell proliferation, predominantly in the choanoderm, but also in the mesohyl. The majority of coral reef species (five) showed between 16.1±15.9% and 19.0±2.0% choanocyte proliferation (mean±SD) after 6 h and the Mediterranean species, C. reniformis, showed 16.6±3.2% after 10 h BrdU-labeling. Monanchora arbuscula showed lower choanocyte proliferation (8.1±3.7%), whereas the mangrove species Mycale microsigmatosa showed relatively higher levels of choanocyte proliferation (70.5±6.6%). Choanocyte proliferation in Haliclona vansoesti was variable (2.8–73.1%). Apoptosis was negligible and not the primary mechanism of cell loss involved in cell turnover. All species investigated produced significant amounts of detritus (2.5–18% detritus bodyweight−1·d−1) and cell shedding was observed in seven out of eight species. The amount of shed cells observed in histological sections may be related to differences in residence time of detritus within canals. Detritus production could not be directly linked to cell shedding due to the degraded nature of expelled cellular debris. We have demonstrated that under steady-state conditions, cell turnover through cell proliferation and cell shedding are common processes to maintain tissue homeostasis in a variety of sponge species from different ecosystems. Cell turnover is hypothesized to be the main underlying mechanism producing sponge-derived detritus, a major trophic resource transferred through sponges in benthic ecosystems, such as coral reefs.

A test of the sponge-loop hypothesis for emergent Caribbean reef sponges

“…Through this process, termed the 'sponge-loop', sponges consume dissolved organic carbon (DOC), and up to 40% of this carbon is subsequently released as particulate organic carbon (POC) in the form of shed cellular detritus that is then assimilated by benthic detritivores and suspension feeders and subsequently passed to higher trophic levels via predation (de Goeij et al 2013, Rix et al 2016. Although the underlying mechanism of detritus production in the spongeloop has yet to be resolved, it is hypothesized that there is a trade-off between sponge growth and detritus production, with the latter linked to rapid cell turnover, primarily of choano cytes, through cell proliferation and cell shedding (de Goeij et al 2009, Alexander et al 2014, 2015; but see Kahn & Leys 2016).…”

Modelling sponge-symbiont metabolism

“…Zhang et al, 2015). They efficiently filter particulate and dissolved material from huge volumes of seawater each day (Reiswig, 1971;Riisgård et al, 1993;Topçu et al, 2010;Turon et al, 1997;Yahel et al, 2003b), making these nutrients available to benthic trophic levels with the release of detritus material (Alexander et al, 2014;de Goeij et al, 2013;de Goeij et al, 2008a;Rix et al, 2016). The efficient cycling of nutrients has long been seen as vital to the high levels of productivity that coral reefs display in low nutrient environments (de Goeij et al, 2013;Hatcher, 1997;Pawlik et al, 2016).…”

“…A carbon balance in Haliclona oculata found that only 34% of the particulate carbon pumped through was used for both respiration and growth, of which 10% was used in biomass synthesis and 90% for energy generation (Koopmans et al, 2009). Much of the nutrients that are converted into biomass appears to be returned to the benthic ecosystem by the shedding of choanocytes, specialised cells that pump seawater from which they filter food (Alexander et al, 2014;de Goeij et al, 2009;Rix et al, 2016;Shore, 1971).…”

“…For instance, marine sponges are valued for their ecosystem services, in particular cycling and retaining nutrients on coral reefs (Alexander et al, 2014;de Goeij et al, 2013;Rix et al, 2016), and as a source of bioactive secondary metabolites with commercial potential (Blunt et al, 2014;Konstantinidis & Tiedje, 2004;Leal et al, 2012;Mehbub et al, 2014;Thomas et al, 2010). It is accepted that the low commercialisation rate of sponge holobiont derived natural products is due to the inability to reliably produce sponge biomass (Belarbi, 2003;Leal et al, 2014;Osinga et al, 1999;Schippers et al, 2012;Sipkema et al, 2005;Wijffels, 2008).…”

“…To maintain a clean and efficient pumping and filtration system, the specialised cells involved, the choanocytes, are shed in large quantities (Alexander et al, 2014;de Goeij et al, 2013;Shore, 1971). A study of five coral reef species of sponge revealed a turnover rate of 16-19% of the choanocyte cell population every six hours (Alexander et al, 2014).…”