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Single-cell visualization indicates direct role of sponge host in uptake of dissolved organic matter
Proceedings of the Royal Society B: Biological Sciences, 2019
Marine sponges are set to become more abundant in many near-future oligotrophic environments, where they play crucial roles in nutrient cycling. Of high importance is their mass turnover of dissolved organic matter (DOM), a heterogeneous mixture that constitutes the largest fraction of organic matter in the ocean and is recycled primarily by bacterial mediation. Little is known, however, about the mechanism that enables sponges to incorporate large quantities of DOM in their nutrition, unlike most other invertebrates. Here, we examine the cellular capacity for direct processing of DOM, and the fate of the processed matter, inside a dinoflagellate-hosting bioeroding sponge that is prominent on Indo-Pacific coral reefs. Integrating transmission electron microscopy with nanoscale secondary ion mass spectrometry, we track 15 N- and 13 C-enriched DOM over time at the individual cell level of an intact sponge holobiont. We show initial high enrichment in the filter-feeding cells of the sp...
Marine Ecology Progress Series
Sponge-microbe symbioses underpin the ecological success of sponges in many aquatic benthic ecosystems worldwide. These symbioses are often described as mutually beneficial, but identifying positive symbiotic interactions and quantifying the contribution of partners to physiological processes is challenging. For example, our understanding of the relative contribution of sponge cells and their microbial symbionts to the uptake and exchange of dissolved organic matter (DOM)—a major component of sponge diet—is limited. Here, we combined host-symbiont cell separation with pulse-chase isotopic labelling in order to trace the uptake of13C- and15Nenriched DOM into sponge cells and microbial symbionts of the encrusting Caribbean spongesHaliclona vansoestiandScopalina ruetzleri, which are low microbial abundance (LMA) species. Sponge cells were responsible for >99% of DOM assimilation during the pulse-chase experiment for both sponge species, while the contribution of symbiotic microbes t...
Scientific Reports
Deep-sea sponges create hotspots of biodiversity and biological activity in the otherwise barren deep-sea. However, it remains elusive how sponge hosts and their microbial symbionts acquire and process food in these food-limited environments. Therefore, we traced the processing (i.e. assimilation and respiration) of 13C- and 15N-enriched dissolved organic matter (DOM) and bacteria by three dominant North Atlantic deep-sea sponges: the high microbial abundance (HMA) demosponge Geodia barretti, the low microbial abundance (LMA) demosponge Hymedesmia paupertas, and the LMA hexactinellid Vazella pourtalesii. We also assessed the assimilation of both food sources into sponge- and bacteria-specific phospholipid-derived fatty acid (PLFA) biomarkers. All sponges were capable of assimilating DOM as well as bacteria. However, processing of the two food sources differed considerably between the tested species: the DOM assimilation-to-respiration efficiency was highest for the HMA sponge, yet u...
Limnology and Oceanography
Sponges are commonly divided into high (HMA) and low (LMA) microbial-abundance species according to the bacterial biomass in their tissue. These two groups reflect distinct aquiferous structures and feeding strategies. In the NW Mediterranean coralligenous community, HMA and LMA sponges are often packed in dense, multispecies assemblages that cover many pinnacles and overhangs. We investigated the metabolism of HMA and LMA species that cohabitate the coralligenous community by sampling in situ the inhaled and exhaled water. Sponges consumed plankton, dissolved organic carbon (DOC), and ammonium in relation to their abundance in ambient water. The plankton retention efficiency was high for all species. DOC was the main source of C for the sponge species, accounting for 90% of the examined sources. Nitrogen fluxes markedly differed between the two groups: plankton was the main source of nitrogen for LMAs that excreted dissolved organic nitrogen (DON) and ammonium. The nitrogenous waste products of LMAs were found to be the major source of nitrogen (up to 97%) for HMAs that efficiently removed DON and ammonium and excreted nitrate. The different capacity of both sponge strategies to use dissolved resources suggests a partial trophic niche separation related to HMA-LMA dichotomy as a mechanism facilitating their dense coexistence in the community. Our findings suggest that a mixed assemblage of sponges (and their associated microbes) is able to utilize the suspended particulate and dissolved material more efficiently than a single species population and may contribute to the understanding of the phenomena of the stability and diversity of dense sponge assemblages in oligotrophic habitats.
Single-cell measurement of ammonium and bicarbonate uptake within a photosymbiotic bioeroding sponge
The ISME journal, 2018
Some of the most aggressive coral-excavating sponges host intracellular dinoflagellates from the genus Symbiodinium, which are hypothesized to provide the sponges with autotrophic energy that powers bioerosion. Investigations of the contribution of Symbiodinium to host metabolism and particularly inorganic nutrient recycling are complicated, however, by the presence of alternative prokaryotic candidates for this role. Here, novel methods are used to study nutrient assimilation and transfer within and between the outer-layer cells of the Indopacific bioeroding sponge Cliona orientalis. Combining stable isotope labelling, transmission electron microscopy (TEM) and nanoscale secondary ion mass spectrometry (NanoSIMS), we visualize and measure metabolic activity at the individual cell level, tracking the fate of N-ammonium and C-bicarbonate within the intact holobiont. We found strong uptake of both inorganic sources (especially C-bicarbonate) by Symbiodinium cells. Labelled organic nut...
Limnology and Oceanography, 2003
The vast majority of organic matter in the world ocean is found in the dissolved pool. However, no evidence has been demonstrated for direct uptake of bulk dissolved organic matter (DOM) by organisms other than bacteria and some invertebrate larvae. The total organic carbon (TOC) is 10-30% higher in coral reefs than in adjacent open waters. The dissolved organic carbon (DOC) accounts for Ͼ90% of the TOC. Using a new in situ technique for clean sampling of the seawater inhaled and exhaled by benthic suspension feeders, we measured directly the removal of DOC in the symbiont-bearing reef sponge Theonella swinhoei. The sponge removed up to 26% (mean Ϯ SD: 12% Ϯ 8%) of the TOC (dissolved and particulate) from the water it filtered during a single passage through its filtration system. Most of the carbon gained by the sponge was from the dissolved pool (10 Ϯ 7 mol C L Ϫ1 ), an order of magnitude greater than the carbon gained from the total living cells (phytoplankton and bacteria) the sponge removed (2 Ϯ 1 mol C L Ϫ1 ). In T. swinhoei, over two-thirds of the sponge biomass consists of symbiotic bacteria, which likely play an important role in DOC uptake. Our findings indicate that the role of DOC in metazoan nutrition and the role of metazoans in DOC cycling may have been grossly underestimated.
The Life of a Sponge in a Sandy Lagoon
Biological Bulletin, 1995
Infaunal soft-bottom invertebrates benefit from the presence of sediment, but sedimentation is potentially harmful for hard-bottom dwellers. Most sponges live on hard bottom, but on coral reefs in the Red Sea, the species Biemna ehrenbergi (Keller, 1889) is found exclusively in soft-bottom lagoons, usually in the shallowest part. This location is a sink environment, which increases the deposition of particulate organic matter. Most of the sponge body is covered by sediment, but the chimneylike siphons protrude from the sediment surface. The sponge is attached to the buried beach-rock, which reduces the risk of dislodgment during storms. Dye injected above and into the sediment revealed, for the first time, a sponge pumping interstitial water (rich with particles and nutrients) into its aquiferous system. Visual examination of plastic replicas of the aquiferous system and electron microscopical analysis of sponge tissue revealed that the transcellular ostia are mostly located on the buried surface of the sponge. The oscula, however, are located on top of the siphons; their elevated position and their ability to close combine to prevent the filtering system outflow from clogging. The transcellular ostia presumably remain open due to cellular mobility. The sponge maintains a large population of bacteriocytes, which contains bacteria of several different species. Some of these bacteria disintegrate, and may be consumed by the sponge.
Particulate organic matter as a food source for a coral reef sponge
Journal of Experimental Biology, 2009
The ability of sponges to feed in diverse (including oligotrophic) ecosystems significantly contributes to their ubiquitous aquatic distribution. It was hypothesized that sponges that harbour small amounts of symbiotic bacteria in their mass feed mainly on particulate organic matter (POM). We examined the nearly symbiont-free (by microscopic observation) filter-feeding Red Sea sponge Negombata magnifica in order to: (a) study removal efficiency of naturally occurring organic particles, (b) measure the total amount of absorbed particulate organic carbon (POC) and nitrogen (PON), and (c) estimate organic carbon and nitrogen flux in this sponge. Total amount of organic carbon and nitrogen in the Gulf of Aqaba was found to be 48.46±5.69gl -1 and 6.45±0.7gl -1 , respectively. While detritus contributed 54% of POC, most PON (84%) came from planktonic microorganisms, mainly prokaryotes. Particle removal efficiency ranged from 99% (the cyanobacterium Synechococcus sp.) to 37% (for eukaryotic cells >8m). On average, N. magnifica ingested 480gCday -1 g -1 (wet mass, WM) sponge and 76.6gNday -1 g -1 sponge. Ingested POC balanced 85% of the spongeʼs energetic demand but more is needed for biomass production because it cannot digest all of the carbon. 54.4±16.1gNday -1 g -1 (WM) nitrogen was excreted as total ammonia nitrogen (TAN); however, nitrogen allowance should be higher because more nitrogen is deposited for sponge biomass during growth. It is hypothesized that the discrepancy in the nutritional requirements should be covered by the sponge absorbing carbon and nitrogen from sources that are not dealt with in the present research, such as dissolved organic carbon and nitrogen. This study highlights the significance of detritus as a carbon source, and prokaryotes as a PON source in sponge feeding.