UvA-DARE ( Digital Academic Repository ) Cell turnover and detritus production in marine sponges from tropical and temperate benthic ecosystems

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-29-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 16.1615. 9% and 19.062. 0% choanocyte proliferation (mean6SD) after 6 h and the Mediterranean species, C. reniformis, showed 16.663. 2% after 10 h BrdU-labeling. Monanchora arbuscula showed lower choanocyte proliferation (8.163.7%), whereas the mangrove species Mycale microsigmatosa showed relatively higher levels of choanocyte proliferation (70.566.6%). 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? d) 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. Citation: Alexander BE, Liebrand K, Osinga R, van der Geest HG, Admiraal W, et al. (2014) Cell Turnover and Detritus Production in Marine Sponges from Tropical and Temperate Benthic Ecosystems. PLoS ONE 9(10): e109486. doi:10.1371/journal.pone. 0109486 Editor: Nicole Webster, Australian Institute of Marine Science, Australia Received June 3, 2014; Accepted September 1, 2014; Published October 7, 2014 Copyright: 2014 Alexander et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability: The authors confirm that all data underlying the findings are fully available without restriction. All data is within the paper, its supporting information files, and raw data is available through Dryad, doi:10.5061/dryad.q4q52. Funding: Porifarma B.V. received funding from the European Union Seventh Framework Programme (FP7/2007–2013) under grant agreement no. KBBE-2010– 266033 to undertake the research leading to these results. Funding was also received from The Innovational Research Incentives Scheme of the Netherlands Organization for Scientific Research (NWO-VENI; 863.10.009; personal grant to JMdG). Mediterranean sampling was partially funded by the grant CGL2010–18466 from the Spanish Government to MR. BEA, RO, and JMdG are affiliated with Porifarma B.V. Porifarma B.V. provided support in the form of salaries for authors BEA, RO, and JMdG, but no employees of Porifarma B.V. other than BEA, RO, and JMdG had any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section. Competing Interests: BEA, RO, and JMdG are affiliated with Porifarma B.V. Porifarma B.V. received funding from the European Union Seventh Framework Programme (FP7/2007–2013) under grant agreement no KBBE-2010-266033 to undertake the research leading to these results. BEA is employed by Porifarma B.V. under grant agreement no KBBE-2010-266033 from the European Union Seventh Framework Programme (FP7/2007–2013). There are no patents, products in development or marketed products to declare. This does not alter the authors’ adherence to all the PLOS ONE policies on sharing data and materials. * Email: B.E. Alexander@uva.nl or britt.e. alexander@gmail.com