In situ Skeletal Growth Rates of the Solitary Cold-Water Coral Tethocyathus endesa From the Chilean Fjord Region

Cold-water corals (CWC) can be found throughout a wide range of latitudes (79°N–78°S). Since they lack the photosymbiosis known for most of their tropical counterparts, they may thrive below the euphotic zone. Consequently, their growth predominantly depends on the prevalent environmental conditions, such as general food availability, seawater chemistry, currents, and temperature. Most CWC communities live in regions that will face CaCO3 undersaturation by the end of the century and are thus predicted to be threatened by ocean acidification (OA). This scenario is especially true for species inhabiting the Chilean fjord system, where present-day carbonate water chemistry already reaches values predicted for the end of the century. To understand the effect of the prevailing environmental conditions on the biomineralization of the CWC Tethocyathus endesa, a solitary scleractinian widely distributed in the Chilean Comau Fjord, a 12-month in situ experiment was conducted. The in situ skeletal growth of the test corals was assessed at two sites using the buoyant weight method. Sites were chosen to cover the naturally present carbonate chemistry gradient, with pH levels ranging between 7.90 ± 0.01 (mean ± SD) and 7.70 ± 0.02, and an aragonite saturation (Ωarag) between 1.47 ± 0.03 and 0.98 ± 0.05. The findings of this study provide one of the first in situ growth assessments of a solitary CWC species, with a skeletal mass increase of 46 ± 28 mg per year and individual, at a rate of 0.03 ± 0.02% day. They also indicate that, although the local seawater chemistry can be assumed to be unfavorable for calcification, growth rates of T. endesa are comparable to other cold-water scleractinians in less corrosive waters (e.g., Lophelia pertusa in the Mediterranean Sea).

Resilience of cold-water coral holobionts to thermal stress

Cold-water corals are threatened by global warming, especially in the Mediterranean Sea where they live close to their upper known thermal limit (i.e. 13°C), yet their response to rising temperatures is not well known. Here, temperature effects on Lophelia pertusa and Madrepora oculata holobionts (i.e. the host and its associated microbiome) were investigated. We found that at warmer seawater temperature (+2°C), L. pertusa showed a modification of its microbiome prior to a change in behaviour, leading to lower energy reserves and skeletal growth, whereas M. oculata was more resilient. At extreme temperature (+4°C), both species quickly lost their specific bacterial signature followed by lower physiological activity prior to death. In addition, our results showing the holobionts' negative response to colder temperatures (−3°C), suggest that Mediterranean corals live close to their thermal optimum. The species-specific response to temperature change highlights that global warming may affect dramatically the main deep-sea reef-builders, which would alter the associated biodiversity and related ecosystem services.

Cold-Water Coral Reefs in the Langenuen Fjord, Southwestern Norway—A Window into Future Environmental Change

Ocean warming and acidification pose serious threats to cold-water corals (CWCs) and the surrounding habitat. Yet, little is known about the role of natural short-term and seasonal environmental variability, which could be pivotal to determine the resilience of CWCs in a changing environment. Here, we provide continuous observational data of the hydrodynamic regime (recorded using two benthic landers) and point measurements of the carbonate and nutrient systems from five Lophelia pertusa reefs in the Langenuen Fjord, southwestern Norway, from 2016 to 2017. In this fjord setting, we found that over a tidal (<24 h) cycle during winter storms, the variability of measured parameters at CWC depths was comparable to the intra-annual variability, demonstrating that single point measurements are not sufficient for documenting (and monitoring) the biogeochemical conditions at CWC sites. Due to seasonal and diurnal forcing, parts of the reefs experienced temperatures up to 4 °C warmer (i.e., >12 °C) than the mean conditions and high CT concentrations of 20 µmol kg−1 over the suggested threshold for healthy CWC reefs (i.e., >2170 µmol kg−1). Combined with hindcast measurements, our findings indicate that these shallow fjord reefs may act as an early hotspot for ocean warming and acidification. We predict that corals in Langenuen will face seasonally high temperatures (>18 °C) and hypoxic and corrosive conditions within this century. Therefore, these fjord coral communities could forewarn us of the coming consequences of climate change on CWC diversity and function.

Host-influenced geochemical signature in the parasitic foraminifera <i>Hyrrokkin sarcophaga</i>

Hyrrokkin sarcophaga is a parasitic foraminifera that is commonly found in cold-water coral reefs where it infests the file clam Acesta excavata and the scleractinian coral Desmophyllum pertusum (formerly known as Lophelia pertusa). Here, we present measurements of the trace element and isotopic composition of these parasitic foraminifera, analyzed by inductively coupled optical emission spectrometry (ICP-OES), electron probe microanalysis (EPMA) and mass spectrometry (gas-source MS and inductively-coupled-plasma MS). Our results reveal that the geochemical signature of H. sarcophaga depends on the host organism it infests. Sr / Ca ratios are 1.1 mmol mol−1 higher in H. sarcophaga that infest D. pertusum, which could be an indication that dissolved host carbonate material is utilized in shell calcification, given that the aragonite of D. pertusum has a naturally higher Sr concentration compared to the calcite of A. excavata. Similarly, we measure 3.1 ‰ lower δ13C and 0.25 ‰ lower δ18O values in H. sarcophaga that lived on D. pertusum, which might be caused by the direct uptake of the host's carbonate material with a more negative isotopic composition or different pH regimes in these foraminifera (pH can exert a control on the extent of CO2 hydration/hydroxylation) due to the uptake of body fluids of the host. We also observe higher Mn / Ca ratios in foraminifera that lived on A. excavata but did not penetrate the host shell compared to specimen that penetrated the shell, which could be interpreted as a change in food source, changes in the calcification rate, Rayleigh fractionation or changing oxygen conditions. While our measurements provide an interesting insight into the calcification process of this unusual foraminifera, these data also indicate that the geochemistry of this parasitic foraminifera is unlikely to be a reliable indicator of paleoenvironmental conditions using Sr / Ca, Mn / Ca, δ18O or δ13C unless the host organism is known and its geochemical composition can be accounted for.

Comparison of Preservation and Extraction Methods on Five Taxonomically Disparate Coral Microbiomes

All animals are host to a multitude of microorganisms that are essential to the animal’s health. Host-associated microbes have been shown to defend against potential pathogens, provide essential nutrients, interact with the host’s immune system, and even regulate mood. However, it can be difficult to preserve and obtain nucleic acids from some host-associated microbiomes, making studying their microbial communities challenging. Corals are an example of this, in part due to their potentially remote, underwater locations, their thick surface mucopolysaccharide layer, and various inherent molecular inhibitors. This study examined three different preservatives (RNAlater, DNA/RNA Shield, and liquid nitrogen) and two extraction methods (the Qiagen PowerBiofilm kit and the Promega Maxwell RBC kit with modifications) to determine if there was an optimum combination for examining the coral microbiome. These methods were employed across taxonomically diverse coral species, including deep-sea/shallow, stony/soft, and zooxanthellate/azooxanthellate: Lophelia pertusa, Paragorgia johnsoni, Montastraea cavernosa, Porites astreoides, and Stephanocoenia intersepta. Although significant differences were found between preservative types and extraction methods, these differences were subtle, and varied in nature from coral species to coral species. Significant differences between coral species were far more profound than those detected between preservative or extraction method. We suggest that the preservative types presented here and extraction methods using a bead-beating step provide enough consistency to compare coral microbiomes across various studies, as long as subtle differences in microbial communities are attributed to dissimilar methodologies. Additionally, the inclusion of internal controls such as a mock community and extraction blanks can help provide context regarding data quality, improving downstream analyses.

Health Screening of the Reef Forming Scleractinian Cold-Water Corals Lophelia pertusa and Madrepora oculata in a Remote Submarine Canyon on the European Continental Margin, NE Atlantic

Temperature and pH can expedite the ability of pathogens to cause diseases in cold-water corals (CWCs). The present study employed a combination of histology and polymerase chain reaction diagnostic techniques to investigate potential pathogens present in the CWCs Lophelia pertusa and Madrepora oculata in the Porcupine Bank Canyon (PBC), NE Atlantic. No pathogen was observed in the Madrepora samples. Neither histology nor standard PCR detected Vibrio spp. in the corals, although using Illumina technology, V. shilonii was observed in some L. pertusa samples in low abundances (0.22%). A Rickettsiales-like organisms (RLOs) occurred at a prevalence of 8.0% and at a low infection intensity of 1 - 4. Lophelia showed a few RLOs infection from the PBC canyon head (2.7%) and high infections in the south branch (5.3%). Similarly, unidentified cells observed in L. pertusa from the south branch (4.0%) were more common than those found in the canyon head (1.3%) with a prevalence of 5.3%. Although the route of pathogen infection is unclear, a likely mode of entry could be associated with particulate availability and the feeding strategies of the scleractinian corals. This suggest that L. pertusa invests energy into an enhanced immune function and reduced susceptibility to global pathogens despite a changing ocean environment.

Host influenced geochemical signature in the parasitic foraminifer Hyrrokkin sarcophaga

Hyrrokkin sarcophaga is a parasitic foraminifer that is commonly found in cold-water coral reefs where it infests the file clam Acesta excavata and the scleractinian coral Lophelia pertusa. Here, we present measurements of the elemental and isotopic composition of this parasitic foraminifer for the first time, analyzed by inductively coupled optical emission spectrometry (ICP-OES), electron probe micro analysis (EPMA) and mass spectrometry (MS).Our results reveal that the geochemical signature of H. sarcophaga depends on the host organism it infests. Sr/Ca ratios are 1.1 mmol mol−1 higher in H. sarcophaga that infest L. pertusa, which could be an indication that dissolved host carbonate material is utilised in shell calcification, given that the aragonite of L. pertusa has a naturally higher Sr concentration compared to the calcite of A. excavata. Similarly, we measure 3.1 ‰ lower δ13C and 0.25 ‰ lower δ18O values in H. sarcophaga that lived on L. pertusa, which might be caused by the direct uptake of the host's carbonate material with a more negative isotopic composition or different pH regimes in these foraminifera (pH can exert a control on the extent of CO2 hydration/hydroxylation) due to the uptake of body fluids of the host. We also observe higher Mn/Ca ratios in foraminifers that lived on A. excavata but did not penetrate the host shell compared to specimen that penetrated the shell, which could be interpreted as a change in food source, changes in the calcification rate, Rayleigh fractionation or changing oxygen conditions.While our measurements provide an interesting insight into the calcification process of this unusual foraminifer, these data also indicate that the geochemistry of this parasitic foraminifer is unlikely to be a reliable indicator of paleoenvironmental conditions using Sr/Ca, Mn/Ca, δ18O or δ13C unless the host organism is known and its geochemical composition can be accounted for.

Cold-water Coral Microbiome and Environmental Microbial Communities in a Remote NE Atlantic Submarine Canyon Setting: Microbial Diversity, Coral Health and Prospects

In the Porcupine Bank Canyon, Lophelia pertusa and Madrepora oculata are the main framework-forming corals producing three dimensional structures which provide a home for a range of benthic fauna and microbial communities. To understand the roles and functions that microbes perform in coral health in the Porcupine Bank Canyon, three groups of samples (corals, sediment and water) were collected between 600–800 m depth. DNA was extracted from these samples and metabarcoding was performed on the V3-V4 region of the 16S RNA gene using Illumina technology. The coral microbiome showed greater microbial diversity than both the surrounding sediment and water communities. The genera Pseudomonas, Pseudoalteramonas and Photobacterium were the bacterial communities conserved at 100% coverage of coral samples whereas at the order-level classification Clostridiales, Bacteroidales, Flavobacteriales, Rhodobacterales and Rickettsiales were in high abundance in all the coral samples. A disproportionate distribution of probiotic and pathogenic bacterial groups at the different levels of classification was observed on the corals. Corals do not appear, at present, to be stressed by climate induced changing environmental conditions in the upper Porcupine Bank Canyon. Overall, the corals in the Porcupine Bank Canyon are in a healthy state despite the detection of pathogenic bacterial groups. However, the current trend of climate change and subsequent deep-sea warming could shift the bacterial composition towards a more dominant pathogenic bacterial community, with serious implications for coral health and stability of this important ecosystem.