Direct visualization of mucus production by the cold-water coral <i>Lophelia pertusa</i> with digital holographic microscopy

<i>Lophelia pertusa</i> is the dominant reef-building organism of cold-water coral reefs, and is known to produce significant amounts of mucus, which could involve an important metabolic cost. Mucus is involved in particle removal and feeding processes, yet the triggers and dynamics of mucus production are currently still poorly described because the existing tools to study these processes are not appropriate. Using a novel microscopic technique—digital holographic microscopy (DHM)–we studied the mucus release of <i>L</i>. <i>pertusa</i> under various experimental conditions. DHM technology permits µm-scale observations and allows the visualization of transparent mucoid substances in real time without staining. Fragments of <i>L</i>. <i>pertusa</i> were first maintained in flow-through chambers without stressors and imaged with DHM, then exposed to various stressors (suspended particles, particulate food and air exposure) and re-imaged. Under non-stressed conditions no release of mucus was observed, whilst mucus strings and sheaths were produced in response to suspended particles (activated charcoal and drill cuttings sediment) i.e. in a stressed condition. Mucus strings and so-called ‘string balls’ were also observed in response to exposure to particulate food (brine shrimp <i>Artemia salina</i>). Upon air-exposure, mucus production was clearly visible once the fragments were returned to the flow chamber. Distinct optical properties such as optical path length difference (OPD) were measured with DHM in response to the various stimuli suggesting that different mucus types are produced by <i>L</i>. <i>pertusa</i>. Mucus produced to reject particles is similar in refractive index to the surrounding seawater, suggesting that the energy content of this mucus is low. In contrast, mucus produced in response to either food particle addition or air exposure had a higher refractive index, suggesting a higher metabolic investment in the production of these mucoid substances. This paper shows for the first time the potential of DHM technology for the detection, characterization and quantification of mucus production through OPD measurements in <i>L</i>. <i>pertusa</i>

Meiofauna metabolism in suboxic sediments: currently overestimated

Oxygen is recognized as a structuring factor of metazoan communities in marine sediments. The importance of oxygen as a controlling factor on meiofauna (32 µm-1 mm in size) respiration rates is however less clear. Typically, respiration rates are measured under oxic conditions, after which these rates are used in food web studies to quantify the role of meiofauna in sediment carbon turnover. Sediment oxygen concentration ([O2]) is generally far from saturated, implying that (1) current estimates of the role of meiofauna in carbon cycling may be biased and (2) meiofaunal organisms need strategies to survive in oxygen-stressed environments. Two main survival strategies are often hypothesized: 1) frequent migration to oxic layers and 2) morphological adaptation. To evaluate these hypotheses, we (1) used a model of oxygen turnover in the meiofauna body as a function of ambient [O2], and (2) performed respiration measurements at a range of [O2] conditions. The oxygen turnover model predicts a tight coupling between ambient [O2] and meiofauna body [O2] with oxygen within the body being consumed in seconds. This fast turnover favors long and slender organisms in sediments with low ambient [O2] but even then frequent migration between suboxic and oxic layers is for most organisms not a viable strategy to alleviate oxygen limitation. Respiration rates of all measured meiofauna organisms slowed down in response to decreasing ambient [O2], with Nematoda displaying the highest metabolic sensitivity for declining [O2] followed by Foraminifera and juvenile Gastropoda. Ostracoda showed a behavioral stress response when ambient [O2] reached a critical level. Reduced respiration at low ambient [O2] implies that meiofauna in natural, i.e. suboxic, sediments must have a lower metabolism than inferred from earlier respiration rates conducted under oxic conditions. The implications of these findings are discussed for the contribution of meiofauna to carbon cycling in marine sediments

Contrasting metabolic strategies of two co‑occurring deep‑sea octocorals

The feeding biology of deep-sea octocorals remains poorly understood, as attention is more often directed to reef building corals. The present study focused on two common deep-water octocoral species in the Azores Archipelago, Dentomuricea aff. meteor and Viminella flagellum, aiming at determining their ability to exploit different food sources. We adopted an experimental approach, with three different food sources, including live phytoplankton, live zooplankton and dissolved organic matter (DOM), that were artificially enriched with 13C and 15N (C and N tracers). The presence of tracers was subsequently followed in the coral tissue, C respiration and particulate organic C and N (POC and PON) release. In both species, feeding with zooplankton resulted in significantly higher incorporation of tracers in all measured variables, compared to the other food sources, highlighting the importance of zooplankton for major physiological processes. Our results revealed contrasting metabolic strategies between the two species, with D. aff. meteor acquiring higher amounts of prey and allocating higher percentage to respiration and release of POC and PON than V. flagellum. Such metabolic differences can shape species fitness and distributions and have further ecological implications on the ecosystem function of communities formed by different octocoral species.Versión del edito

Hydrothermal activity, functional diversity and chemoautotrophy are major drivers of seafloor carbon cycling

Hydrothermal vents are highly dynamic ecosystems and are unusually energy rich in the deep-sea. In situ hydrothermal-based productivity combined with sinking photosynthetic organic matter in a soft-sediment setting creates geochemically diverse environments, which remain poorly studied. Here, we use comprehensive set of new and existing field observations to develop a quantitative ecosystem model of a deep-sea chemosynthetic ecosystem from the most southerly hydrothermal vent system known. We find evidence of chemosynthetic production supplementing the metazoan food web both at vent sites and elsewhere in the Bransfield Strait. Endosymbiont-bearing fauna were very important in supporting the transfer of chemosynthetic carbon into the food web, particularly to higher trophic levels. Chemosynthetic production occurred at all sites to varying degrees but was generally only a small component of the total organic matter inputs to the food web, even in the most hydrothermally active areas, owing in part to a low and patchy density of vent-endemic fauna. Differences between relative abundance of faunal functional groups, resulting from environmental variability, were clear drivers of differences in biogeochemical cycling and resulted in substantially different carbon processing patterns between habitats

Carbon cycling in the deep eastern North Pacific benthic food web: Investigating the effect of organic carbon input

The deep ocean benthic environment plays a role in long-term carbon sequestration. Understanding carbon cycling in the deep ocean floor is critical to evaluate the impact of changing climate on the oceanic systems. Linear inverse modeling was used to quantify carbon transfer between compartments in the benthic food web at a long time-series study site in the abyssal northeastern Pacific (Station M). Linear inverse food web models were constructed for three separate years in the time-series when particulate organic carbon (POC) flux was relatively high (1990: 0.63 mean mmol C m?2 d?1), intermediate (1995: 0.24) and low (1996: 0.12). Carbon cycling in all years was dominated by the flows involved in the microbial loop; dissolved organic carbon uptake by microbes (0.80–0.95 mean mmol C m?2 d?1), microbial respiration (0.52–0.61), microbial biomass dissolution (0.09–0.18) and the dissolution of refractory detritus (0.46–0.65). Moreover, the magnitude of carbon flows involved in the microbial loop changed in relation to POC input, with a decline in contribution during the high POC influxes, such as those recently experienced at Station M. Results indicate that during high POC episodic pulses the role of faunal mediated carbon cycling would increase. Semi-labile detritus dominates benthic faunal diets and the role of labile detritus declined with increased total POC input. Linear inverse modeling represents an effective framework to analyze high-resolution time-series data and demonstrate the impact of climate change on the deep ocean carbon cycle in a coastal upwelling system

The structure and functional roles of tidal flat meiobenthos

Meiofauna comprise the smallest multicellular and largest unicellular metazoans in benthic food webs. They are highly abundant and species-rich, yet essential aspects of the factors driving their community structure and abundance remain poorly understood. Similarly, their functional roles in benthic carbon cycling remain poorly characterized and even more poorly quantified. In the frame of two projects, we addressed questions regarding both the biotic and abiotic factors that drive meiobenthic assemblage structure, and their roles in benthic carbon cycling. Our research involved an intricate combination of manipulative laboratory experiments and field work, the latter mostly focusing on the intertidal flats bordering the Paulina salt marsh in the Scheldt estuary. The results add considerably to our understanding of the factors that drive meiobenthic assemblage structure. They clearly demonstrate that biotic interactions among different meiofauna, and between meio- and macrofauna, are extremely important and moderate the impacts of prominent abiotic drivers of assemblage structure such as granulometry and oxygen availability. From a functional point of view, we demonstrated that tidal flat meiofauna rely predominantly on carbon derived from in situ primary production by microphytobenthos. Quantification of grazing rates of meiofauna on microphytobenthos and benthic bacteria does not, however, point at an important direct contribution of meiofauna to benthic carbon cycling. The role of meiobenthic species diversity remains to be established, but laboratory experiments into the role of nematodes in OM decomposition reveal that in addition to species identity, species diversity does have a significant, yet largely unpredictable effect on OM decomposition rates

Changing the choice from dialysis to conservative care or vice versa in older patients with advanced chronic kidney disease

Nephrolog

Reef sponges facilitate the transfer of coral-derived organic matter to their associated fauna via the sponge loop

The high biodiversity of coral reefs results in complex trophic webs where energy and nutrients are transferred between species through a multitude of pathways. Here, we hypothesize that reef sponges convert the dissolved organic matter released by benthic primary producers (e.g. corals) into particulate detritus that is transferred to sponge-associated detritivores via the sponge loop pathway. To test this hypothesis, we conducted stable isotope (13C and15N) tracer experiments to investigate the uptake and transfer of coral-derived organic matter from the sponges Mycale fistulifera and Negombata magnifica to 2 types of detritivores commonly associated with sponges: ophiuroids (Ophiothrix savignyi and Ophiocoma scolopendrina) and polychaetes (Polydorella smurovi). Findings revealed that the organic matter naturally released by the corals was indeed readily assimilated by both sponges and rapidly released again as sponge detritus. This detritus was subsequently consumed by the detritivores, demonstrating transfer of coral-derived organic matter from sponges to their associated fauna and confirming all steps of the sponge loop. Thus, sponges provide a trophic link between corals and higher trophic levels, thereby acting as key players within reef food webs

Unravelling the versatile feeding and metabolic strategies of the cold-water ecosystem engineer Spongosorites coralliophaga (Stephens, 1915)

Thanks to Bill Richardson (Master) and the crew of the Royal Research Ship “James Cook” during the JC073 “Changing Oceans” expedition, Will Handley and the Holland-I ROV team. Also thanks to Dr Christina Mueller and Dr Evina Gontikaki for their guidance on experimental set-up and sample preparation for stable isotope analysis. Funding for the JC073 cruise was provided by the Natural Environment Research Council (NERC) UK Ocean Acidification (UKOA) research programme’s Benthic Consortium project (NE/H017305/1 to J Murray Roberts). Funding for the field work and analytical costs was provided by the Marine Alliance for Science and Technology for Scotland (MASTS) (Biodiversity Grant to UW, 140 SF10003-10, Deep-Sea Forum Small Grant DSSG4 awarded to GK) and by the Netherlands Organisation for Scientific Research (awarded to DvO). GK was funded by a MASTS PhD scholarship. The ATLAS project has received funding from the European Union’s Horizon 2020 research and innovation programme under grant agreement No 678760 (ATLAS). This output reflects only the author’s views, and the European Union cannot be held responsible for any use that may be made of the information contained therein. The funding sources had no involvement in study design, the collection, analysis and interpretation of data, in the writing of the report, and in the decision to submit the article for publication. The authors would like to thank the two reviewers of the manuscript for their constructive comments.Peer reviewedPostprin

Heterotrophy in the earliest gut: a single-cell view of heterotrophic carbon and nitrogen assimilation in sponge-microbe symbioses

Sponges are the oldest known extant animal-microbe symbiosis. These ubiquitous benthic animals play an important role in marine ecosystems in the cycling of dissolved organic matter (DOM), the largest source of organic matter on Earth. The conventional view on DOM cycling through microbial processing has been challenged by the interaction between this efficient filter-feeding host and its diverse and abundant microbiome. Here we quantify, for the first time, the role of host cells and microbial symbionts in sponge heterotrophy. We combined stable isotope probing and nanoscale secondary ion mass spectrometry to compare the processing of different sources of DOM (glucose, amino acids, algal-produced) and particulate organic matter (POM) by a high-microbial abundance (HMA) and low-microbial abundance (LMA) sponge with single-cell resolution. Contrary to common notion, we found that both microbial symbionts and host choanocyte (i.e. filter) cells and were active in DOM uptake. Although all DOM sources were assimilated by both sponges, higher microbial biomass in the HMA sponge corresponded to an increased capacity to process a greater variety of dissolved compounds. Nevertheless, in situ feeding data demonstrated that DOM was the primary carbon source for both the LMA and HMA sponge, accounting for ~90% of their heterotrophic diets. Microbes accounted for the majority (65–87%) of DOM assimilated by the HMA sponge (and ~60% of its total heterotrophic diet) but <5% in the LMA sponge. We propose that the evolutionary success of sponges is due to their different strategies to exploit the vast reservoir of DOM in the ocean