Abstract
Benthic–pelagic coupling through suspension feeders and their detrital pathways is integral to carbon transport in oceans. In food-poor ecosystems however, a novel mechanism of carbon recycling has been proposed that involves direct uptake of dissolved carbon by suspension feeders followed by shedding of cells as particulate carbon. We studied cell replacement rates in a range of cold-water sponge species to determine how universal this mechanism might be. We show that cell replacement rates of feeding epithelia in explants vary from 30 hours up to 7 days, and change during different seasons and life-history stages. We also found that feeding epithelia are not replaced through direct replication but instead arise from a population of stem cells that differentiate and integrate into epithelial tissues. Our results reveal a surprising amount of complexity in the control of cell processes in sponges, with cell turnover depending on environmental conditions and using stem cells as rate-limiting mechanisms. Our results also suggest that for species in cold water with high particulate organic matter, cell turnover is not the mechanism delivering carbon flux to surrounding communities.
Highlights
Suspension feeders transfer carbon to the benthos by capturing and concentrating plankton from the water column [1], but exactly how carbon is transferred is still not clear
The cell cycle was shortest in the calcareous sponge Sy. coactum at 30 h and much longer in adult Sp. lacustris, H. mollis and A. vastus
Choanocytes and amoeboid cells from the mesohyl labelled with equal frequency in H. mollis, whereas two to five times more choanocytes were labelled than mesohyl cells in Sp. lacustris
Summary
Suspension feeders transfer carbon to the benthos by capturing and concentrating plankton from the water column [1], but exactly how carbon is transferred is still not clear. A fourth pathway has come to light that involves uptake of DOM by animals directly (such as sponges) and sloughing of tissues [2] The latter has been termed the ‘sponge loop’ and may be so substantial that it could provide all of Darwin’s missing carbon in oligotrophic coral reefs [2]. This idea has resonated with a wide range of fields from ecology [3,4] to natural products and drug discovery [5], evolutionary developmental biology [6,7], 2016 The Authors.
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