Survival under conditions of variable food availability: Resource utilization and storage in the cold-water coral Lophelia pertusa

Cold‐water coral (CWC) reefs are hotspots of biodiversity and productivity in the deep sea, but their distribution is limited by the availability of food, which undergoes complex local and temporal variability. We studied the resource utilization, metabolism, and tissue storage of CWC Lophelia pertusa during an experimentally simulated 3‐day food pulse, of 13C15N‐enriched phytodetritus, followed by a 4‐week food deprivation. Oxygen consumption (0.145 μmol O2 [mmol organic carbon {OC}]−1 h−1), release of particulate organic matter (0.029 μmol particulate organic carbon [POC] [mmol OC]−1 h−1 and 0.005 μmol particulate organic nitrogen [mmol OC]−1 h−1), ammonium excretion (0.004 μmol NH4+ [mmol OC]−1 h−1), tissue C and N content, and fatty acid (FA) and amino acid composition did not change significantly during the experiment. Metabolization of the labeled phytodetritus, however, underwent distinct temporal dynamics. Initially, L. pertusa preferentially used phytodetritus‐derived C for respiration (2.2 ± 0.36 nmol C [mmol OC]−1 h−1) and mucus production (0.94 ± 0.52 nmol C [mmol OC]−1 h−1), but those tracer fluxes declined exponentially to <20% within 2 weeks after feeding and then remained stable, indicating that the remainder of the incorporated phytodetritus had entered a tissue pool with lower turnover. Analysis of 13C in individual FAs revealed a mismatch between the FAs incorporated from phytodetritus and the FA requirements of the coral. We suggest that feeding on other resources, such as lipid‐rich zooplankton, could fill this deficiency. A release of 10% of their total OC as respired C and POC during the 4‐week food deprivation underlines the importance of regular food pulses for CWC reefs.publishedVersio

On the paradox of thriving cold-water coral reefs in the food-limited deep sea

The deep sea is amongst the most food-limited habitats on Earth, as only a small fraction (<4%) of the surface primary production is exported below 200 m water depth. Here, cold-water coral (CWC) reefs form oases of life: their biodiversity compares with tropical coral reefs, their biomass and metabolic activity exceed other deep-sea ecosystems by far. We critically assess the paradox of thriving CWC reefs in the food-limited deep sea, by reviewing the literature and open-access data on CWC habitats. This review shows firstly that CWCs typically occur in areas where the food supply is not constantly low, but undergoes pronounced temporal variation. High currents, downwelling and/or vertically migrating zooplankton temporally boost the export of surface organic matter to the seabed, creating ‘feast’ conditions, interspersed with ‘famine’ periods during the non-productive season. Secondly, CWCs, particularly the most common reef-builder Desmophyllum pertusum (formerly known as Lophelia pertusa), are well adapted to these fluctuations in food availability. Laboratory and in situ measurements revealed their dietary flexibility, tissue reserves, and temporal variation in growth and energy allocation. Thirdly, the high structural and functional diversity of CWC reefs increases resource retention: acting as giant filters and sustaining complex food webs with diverse recycling pathways, the reefs optimise resource gains over losses. Anthropogenic pressures, including climate change and ocean acidification, threaten this fragile equilibrium through decreased resource supply, increased energy costs, and dissolution of the calcium-carbonate reef framework. Based on this review, we suggest additional criteria to judge the health of CWC reefs and their chance to persist in the future.publishedVersio

Recycling pathways in cold-water coral reefs: Use of dissolved organic matter and bacteria by key suspension feeding taxa

Cold-water coral (CWC) reefs are one of the most diverse and productive ecosystems in the deep sea. Especially in periods of seasonally-reduced phytodetritus food supply, their high productivity may depend on the recycling of resources produced on the reef, such as dissolved organic matter (DOM) and bacteria. Here, we demonstrate that abundant suspension feeders Geodia barretti (high-microbial-abundance sponge), Mycale lingua (low-microbial-abundance sponge) and Acesta excavata (bivalve) are able to utilize 13C-enriched (diatom-derived) DOM and bacteria for tissue growth and respiration. While DOM was an important potential resource for all taxa, utilization of bacteria was higher for the sponges as compared to the bivalve, indicating a particle-size differentiation among the investigated suspension feeders. Interestingly, all taxa released 13C-enriched particulate organic carbon, which in turn may feed the detritus pathway on the reef. Especially A. excavata produced abundant (pseudo-)fecal droppings. A second stable-isotope tracer experiment revealed that detritivorous ophiuroids utilized these droppings. The high resource flexibility of dominant reef suspension feeders, and the efficient recycling of their waste products by the detritivore community, may provide important pathways to maintain the high productivity on cold-water coral reefs, especially in periods of low external food supply.publishedVersio

Reef communities associated with ‘dead’ cold-water coral framework drive resource retention and recycling in the deep sea

Cold-water coral (CWC) reefs create hotspots of metabolic activity in the deep sea, in spite of the limited supply of fresh organic matter from the ocean surface (i.e. phytodetritus). We propose that ‘dead’ coral framework, which harbours diverse faunal and microbial communities, boosts the metabolic activity of the reefs, through enhanced resource retention and recycling. Analysis of a video transect across a 700-540 m-deep CWC mound (Rockall Bank, North-East Atlantic) revealed a high benthic cover of dead framework (64%). Box-cored fragments of dead framework were incubated on-board and showed oxygen consumption rates of 0.078–0.182 μmol O2 (mmol organic carbon, i.e. OC)-1 h-1, indicating a substantial contribution to the total metabolic activity of the CWC reef. During the incubations, it was shown that the framework degradation stage influences nitrogen (re)cycling, corresponding to differences in community composition. New (less-degraded) framework released ammonium (0.005 ± 0.001 μmol NH4+ (mmol OC) 1 h 1), probably due to the activity of ammonotelic macrofauna. In contrast, old (more-degraded) framework released nitrate (0.015 ± 0.008 μmol NO3- (mmol OC)- 1 h- 1), indicating that nitrifying microorganisms recycled fauna-excreted ammonium to nitrate. Furthermore, the framework community removed natural dissolved organic matter (DOM) from the incubation water (0.005–0.122 μmol C (mmol OC)- 1 h- 1). Additional feeding experiments showed that all functional groups and macrofauna taxa of the framework community incorporated 13C-enriched (‘labelled’) DOM, indicating widespread DOM uptake and recycling. Finally, the framework effectively retained 13C-enriched phytodetritus, (a) by physical retention on the biofilm-covered surface and (b) by biological filtration through suspension-feeding fauna. We therefore suggest that the dead framework acts as a ‘filtration-recycling factory’ that enhances the metabolic activity of CWC reefs. The exposed framework, however, is particularly vulnerable to ocean acidification, jeopardizing this important aspect of CWC reef functioning

Tiger reefs: Self‐organized regular patterns in deep‐sea cold‐water coral reefs

Complexity theory predicts that self-organized, regularly patterned ecosystems store more biomass and are more resilient than spatially uniform systems. Self-organized ecosystems are well-known from the terrestrial realm, with “tiger bushes” being the archetypical example and mussel beds and tropical coral reefs the marine examples. We here identify regular spatial patterns in cold-water coral reefs (nicknamed “tiger reefs”) from video transects and argue that these are likely the result of self-organization. We used variograms and Lomb–Scargle analysis of seven annotated video transects to analyze spatial patterns in live coral and dead coral (i.e., skeletal remains) cover at the Logachev coral mound province (NE Atlantic Ocean) and found regular spatial patterns with length scales between 62 and 523 m in live and dead coral distribution along these transects that point to self-organization of cold-water coral reefs. Self-organization theory shows that self-organized ecosystems can withstand large environmental changes by adjusting their spatial configuration. We found indications that cold-water corals can similarly adjust their spatial configuration, possibly providing resilience in the face of climate change. Dead coral framework remains in the environment for extended periods of time, providing a template for spatial patterns that facilitates live coral recovery. The notion of regular spatial patterns in cold-water coral reefs is interesting for cold-water coral restoration, as transplantation will be more successful when it follows the patterns that are naturally present. This finding also underlines that anthropogenic effects such as ocean acidification and bottom trawling that destroy the dead coral template undermine cold-water coral resilience. Differences in the pattern periodicities of live and dead coral cover further present an interesting new angle to investigate past and present environmental conditions in cold-water coral reefs

Tiger reefs: Self-organized regular patterns in deep-sea cold-water coral reefs

Abstract Complexity theory predicts that self-organized, regularly patterned ecosystems store more biomass and are more resilient than spatially uniform systems. Self-organized ecosystems are well-known from the terrestrial realm, with “tiger bushes” being the archetypical example and mussel beds and tropical coral reefs the marine examples. We here identify regular spatial patterns in cold-water coral reefs (nicknamed “tiger reefs”) from video transects and argue that these are likely the result of self-organization. We used variograms and Lomb–Scargle analysis of seven annotated video transects to analyze spatial patterns in live coral and dead coral (i.e., skeletal remains) cover at the Logachev coral mound province (NE Atlantic Ocean) and found regular spatial patterns with length scales between 62 and 523 m in live and dead coral distribution along these transects that point to self-organization of cold-water coral reefs. Self-organization theory shows that self-organized ecosystems can withstand large environmental changes by adjusting their spatial configuration. We found indications that cold-water corals can similarly adjust their spatial configuration, possibly providing resilience in the face of climate change. Dead coral framework remains in the environment for extended periods of time, providing a template for spatial patterns that facilitates live coral recovery. The notion of regular spatial patterns in cold-water coral reefs is interesting for cold-water coral restoration, as transplantation will be more successful when it follows the patterns that are naturally present. This finding also underlines that anthropogenic effects such as ocean acidification and bottom trawling that destroy the dead coral template undermine cold-water coral resilience. Differences in the pattern periodicities of live and dead coral cover further present an interesting new angle to investigate past and present environmental conditions in cold-water coral reefs

On the paradox of thriving cold‐water coral reefs in the food‐limited deep sea

The deep sea is amongst the most food‐limited habitats on Earth, as only a small fraction of the surface primary production is exported below 200 m water depth. Here, cold‐water coral (CWC) reefs form oases of life: their biodiversity compares with tropical coral reefs, their biomass and metabolic activity exceed other deep‐sea ecosystems by far. We critically assess the paradox of thriving CWC reefs in the food‐limited deep sea, by reviewing the literature and open‐access data on CWC habitats. This review shows firstly that CWCs typically occur in areas where the food supply is not constantly low, but undergoes pronounced temporal variation. High currents, downwelling and/or vertically migrating zooplankton temporally boost the export of surface organic matter to the seabed, creating ‘feast’ conditions, interspersed with ‘famine’ periods during the non‐productive season. Secondly, CWCs, particularly the most common reef‐builder &lt;jats:italic&gt;Desmophyllum pertusum&lt;/jats:italic&gt; (formerly known as &lt;jats:italic&gt;Lophelia pertusa&lt;/jats:italic&gt;), are well adapted to these fluctuations in food availability. Laboratory and measurements revealed their dietary flexibility, tissue reserves, and temporal variation in growth and energy allocation. Thirdly, the high structural and functional diversity of CWC reefs increases resource retention: acting as giant filters and sustaining complex food webs with diverse recycling pathways, the reefs optimise resource gains over losses. Anthropogenic pressures, including climate change and ocean acidification, threaten this fragile equilibrium through decreased resource supply, increased energy costs, and dissolution of the calcium‐carbonate reef framework. Based on this review, we suggest additional criteria to judge the health of CWC reefs and their chance to persist in the future

On the paradox of thriving cold‐water coral reefs in the food‐limited deep sea

The deep sea is amongst the most food‐limited habitats on Earth, as only a small fraction of the surface primary production is exported below 200 m water depth. Here, cold‐water coral (CWC) reefs form oases of life: their biodiversity compares with tropical coral reefs, their biomass and metabolic activity exceed other deep‐sea ecosystems by far. We critically assess the paradox of thriving CWC reefs in the food‐limited deep sea, by reviewing the literature and open‐access data on CWC habitats. This review shows firstly that CWCs typically occur in areas where the food supply is not constantly low, but undergoes pronounced temporal variation. High currents, downwelling and/or vertically migrating zooplankton temporally boost the export of surface organic matter to the seabed, creating ‘feast’ conditions, interspersed with ‘famine’ periods during the non‐productive season. Secondly, CWCs, particularly the most common reef‐builder &lt;jats:italic&gt;Desmophyllum pertusum&lt;/jats:italic&gt; (formerly known as &lt;jats:italic&gt;Lophelia pertusa&lt;/jats:italic&gt;), are well adapted to these fluctuations in food availability. Laboratory and measurements revealed their dietary flexibility, tissue reserves, and temporal variation in growth and energy allocation. Thirdly, the high structural and functional diversity of CWC reefs increases resource retention: acting as giant filters and sustaining complex food webs with diverse recycling pathways, the reefs optimise resource gains over losses. Anthropogenic pressures, including climate change and ocean acidification, threaten this fragile equilibrium through decreased resource supply, increased energy costs, and dissolution of the calcium‐carbonate reef framework. Based on this review, we suggest additional criteria to judge the health of CWC reefs and their chance to persist in the future

A site assessment tool for inpatient controlled human infection models for enteric disease pathogens

The use of the controlled human infection model to facilitate product development and to advance understanding of host-pathogen interactions is of increasing interest. While administering a virulent (or infective) organism to a susceptible host necessitates an ongoing evaluation of safety and ethical considerations, a central theme in conducting these studies in a safe and ethical manner that yields actionable data is their conduct in facilities well-suited to address their unique attributes. To that end, we have developed a framework for evaluating potential sites in which to conduct inpatient enteric controlled human infection model to ensure consistency and increase the likelihood of success.publishedVersio

Refinement of the GINGF3 locus for hereditary gingival fibromatosis

Hereditary gingival fibromatosis (HGF) is a rare, clinically variable disorder characterized by slowly progressive fibrous overgrowth of the gingiva. Four gene loci have been mapped for autosomal dominant non-syndromic HGF (adHGF). The molecular basis of adHGF remains largely unknown, with only a single SOS1 gene mutation identified so far at the gingival fibromatosis 1 (GINGF1) locus in one family. We identified an adHGF family with ten affected individuals in whom onset of gingival fibromatosis concurred with the eruption of the primary teeth. In order to identify the molecular basis in this family, we tested for linkage of the disease to known adHGF loci. A maximal multipoint logarithm of the odds score of 3.91 was obtained with marker D2S390 (θ = 0) at the GINGF3 locus on chromosome 2p23.3–p22.3, and linkage to other known loci was excluded. Sequencing two candidate genes, ALK and C2orf18, and a single nucleotide polymorphisms array analysis did not reveal a mutation or copy number variation in a patient from the family. We refined the GINGF3 locus to a 6.56-cM, 8.27-Mb region containing 112 known and hypothetical genes, and our data and a search of the literature suggest that GINGF3 is a major adHGF locus