New records of Provanna (Gastropoda, Provannidae) from the Costa Rica Margin and an identification key for the genus.

Consistent species identification is foundational to biological research and requires coordination among a diversity of researchers and institutions. However, such consistency may be hindered for rare organisms where specimens, identification resources, and taxonomic experts are few. This is often the case for deep-sea taxonomic groups. For example, the deep-sea gastropod genus Provanna Dall, 1918 is common at chemosynthetic sites throughout the world's oceans, yet no formal guide to these species has yet been produced. Recent exploration has recovered new specimens of Provanna from hydrocarbon seeps off the Pacific Costa Rica Margin. The current work assesses the species identity of these specimens using shell morphology, radular morphology, and genetic barcoding (mitochondrial CO1 and nuclear H3). Records of occurrence for P.laevis Warén & Ponder, 1991, P.ios Warén & Bouchet, 1986, and P.pacifica Warén & Bouchet, 1986 are herein presented from the Costa Rica Margin. A critical taxonomic review of the 29 extant species within this genus was conducted and their genetic, morphological, and biogeographical distinction assessed. In this review, genetic and morphological support was found for nearly all current species delineations except for P.glabraOkutani et al., 1992, syn. nov. and P.laevis, syn. nov., which are herein synonymized to P.laevis, and for P.ios, syn. nov. and P.goniata Warén & Bouchet, 1986, syn. nov., which are synonymized to P.ios. Finally, the first species identification key for the extant species in this genus is presented. This work clarifies the taxonomy and systematics of this deep-sea gastropod genus and contributes a novel polytomous key for use in future research.

Expanding our view of the cold-water coral niche and accounting of the ecosystem services of the reef habitat.

Coral reefs are iconic ecosystems that support diverse, productive communities in both shallow and deep waters. However, our incomplete knowledge of cold-water coral (CWC) niche space limits our understanding of their distribution and precludes a complete accounting of the ecosystem services they provide. Here, we present the results of recent surveys of the CWC mound province on the Blake Plateau off the U.S. east coast, an area of intense human activity including fisheries and naval operations, and potentially energy and mineral extraction. At one site, CWC mounds are arranged in lines that total over 150 km in length, making this one of the largest reef complexes discovered in the deep ocean. This site experiences rapid and extreme shifts in temperature between 4.3 and 10.7 °C, and currents approaching 1 m s-1. Carbon is transported to depth by mesopelagic micronekton and nutrient cycling on the reef results in some of the highest nitrate concentrations recorded in the region. Predictive models reveal expanded areas of highly suitable habitat that currently remain unexplored. Multidisciplinary exploration of this new site has expanded understanding of the cold-water coral niche, improved our accounting of the ecosystem services of the reef habitat, and emphasizes the importance of properly managing these systems.

Corals and sponges are hotspots of reactive oxygen species in the deep sea.

Reactive oxygen species (ROS) are central to diverse biological processes through which organisms respond to and interact with their surroundings. Yet, a lack of direct measurements limits our understanding of the distribution of ROS in the ocean. Using a recently developed in situ sensor, we show that deep-sea corals and sponges produce the ROS superoxide, revealing that benthic organisms can be sources and hotspots of ROS production in these environments. These findings confirm previous contentions that extracellular superoxide production by corals can be independent of the activity of photosynthetic symbionts. The discovery of deep-sea corals and sponges as sources of ROS has implications for the physiology and ecology of benthic organisms and introduces a previously overlooked suite of redox reactants at depth.

Venturing into the unfathomableThe Underworld: Journeys to the Depths of the Ocean Susan Casey Doubleday, 2023. 352 pp.

A writer examines our evolving relationship with the deep ocean.

Deep-sea impacts of climate interventions.

Ocean manipulation to mitigate climate change may harm deep-sea ecosystems.

Genome assembly of the deep-sea coral Lophelia pertusa.

Like their shallow-water counterparts, cold-water corals create reefs that support highly diverse communities, and these structures are subject to numerous anthropogenic threats. Here, we present the genome assembly of Lophelia pertusa from the southeastern coast of the USA, the first one for a deep-sea scleractinian coral species. We generated PacBio continuous long reads data for an initial assembly and proximity ligation data for scaffolding. The assembly was annotated using evidence from transcripts, proteins, and ab initio gene model predictions. This assembly is comparable to high-quality reference genomes from shallow-water scleractinian corals. The assembly comprises 2,858 scaffolds (N50 1.6 Mbp) and has a size of 556.9 Mbp. Approximately 57% of the genome comprises repetitive elements and 34% of coding DNA. We predicted 41,089 genes, including 91.1% of complete metazoan orthologs. This assembly will facilitate investigations into the ecology of this species and the evolution of deep-sea corals.

Capacity of deep-sea corals to obtain nutrition from cold seeps aligned with microbiome reorganization.

Cold seeps in the deep sea harbor various animals that have adapted to utilize seepage chemicals with the aid of chemosynthetic microbes that serve as primary producers. Corals are among the animals that live near seep habitats and yet, there is a lack of evidence that corals gain benefits and/or incur costs from cold seeps. Here, we focused on Callogorgia delta and Paramuricea sp. type B3 that live near and far from visual signs of currently active seepage at five sites in the deep Gulf of Mexico. We tested whether these corals rely on chemosynthetically-derived food in seep habitats and how the proximity to cold seeps may influence; (i) coral colony traits (i.e., health status, growth rate, regrowth after sampling, and branch loss) and associated epifauna, (ii) associated microbiome, and (iii) host transcriptomes. Stable isotope data showed that many coral colonies utilized chemosynthetically derived food, but the feeding strategy differed by coral species. The microbiome composition of C. delta, unlike Paramuricea sp., varied significantly between seep and non-seep colonies and both coral species were associated with various sulfur-oxidizing bacteria (SUP05). Interestingly, the relative abundances of SUP05 varied among seep and non-seep colonies and were strongly correlated with carbon and nitrogen stable isotope values. In contrast, the proximity to cold seeps did not have a measurable effect on gene expression, colony traits, or associated epifauna in coral species. Our work provides the first evidence that some corals may gain benefits from living near cold seeps with apparently limited costs to the colonies. Cold seeps provide not only hard substrate but also food to cold-water corals. Furthermore, restructuring of the microbiome communities (particularly SUP05) is likely the key adaptive process to aid corals in utilizing seepage-derived carbon. This highlights that those deep-sea corals may upregulate particular microbial symbiont communities to cope with environmental gradients.

Distribution and predicted climatic refugia for a reef-building cold-water coral on the southeast US margin.

Climate change is reorganizing the planet's biodiversity, necessitating proactive management of species and habitats based on spatiotemporal predictions of distributions across climate scenarios. In marine settings, climatic changes will predominantly manifest via warming, ocean acidification, deoxygenation, and changes in hydrodynamics. Lophelia pertusa, the main reef-forming coral present throughout the deep Atlantic Ocean (>200 m), is particularly sensitive to such stressors with stark reductions in suitable habitat predicted to accrue by 2100 in a business-as-usual scenario. However, with new occurrence data for this species along with higher-resolution bathymetry and climate data, it may be possible to locate further climatic refugia. Here, we synthesize new and published biogeographic, geomorphological, and climatic data to build ensemble, multi-scale habitat suitability models for L. pertusa on the continental margin of the southeast United States (SEUS). We then project these models in two timepoints (2050, 2100) and four climate change scenarios to characterize the occurrence probability of this critical cold-water coral (CWC) habitat now and in the future. Our models reveal the extent of reef habitat in the SEUS and corroborate it as the largest currently known essentially continuous CWC reef province on earth, and also predict abundance of L. pertusa to identify key areas, including those outside areas currently protected from bottom-contact fishing. Drastic reductions in L. pertusa climatic suitability index emerged primarily after 2050 and were concentrated at the shallower end (<~550 m) of the regional distribution under the Gulf Stream main axis. Our results thus suggest a depth-driven climate refuge effect where deeper, cooler reef sites experience lesser declines. The strength of this effect increases with climate scenario severity. Taken together, our study has implications for the regional and global management of this species, portending changes in the biodiversity reliant on CWC habitats and the critical ecosystem services they provide.

Temperature Controls eDNA Persistence across Physicochemical Conditions in Seawater.

Environmental DNA (eDNA) quantification and sequencing are emerging techniques for assessing biodiversity in marine ecosystems. Environmental DNA can be transported by ocean currents and may remain at detectable concentrations far from its source depending on how long it persist. Thus, predicting the persistence time of eDNA is crucial to defining the spatial context of the information derived from it. To investigate the physicochemical controls of eDNA persistence, we performed degradation experiments at temperature, pH, and oxygen conditions relevant to the open ocean and the deep sea. The eDNA degradation process was best explained by a model with two phases with different decay rate constants. During the initial phase, eDNA degraded rapidly, and the rate was independent of physicochemical factors. During the second phase, eDNA degraded slowly, and the rate was strongly controlled by temperature, weakly controlled by pH, and not controlled by dissolved oxygen concentration. We demonstrate that marine eDNA can persist at quantifiable concentrations for over 2 weeks at low temperatures (≤10 °C) but for a week or less at ≥20 °C. The relationship between temperature and eDNA persistence is independent of the source species. We propose a general temperature-dependent model to predict the maximum persistence time of eDNA detectable through single-species eDNA quantification methods.

Relationships between biodiversity and ecosystem functioning proxies strengthen when approaching chemosynthetic deep-sea methane seeps.

As biodiversity loss accelerates globally, understanding environmental influence over biodiversity-ecosystem functioning (BEF) relationships becomes crucial for ecosystem management. Theory suggests that resource supply affects the shape of BEF relationships, but this awaits detailed investigation in marine ecosystems. Here, we use deep-sea chemosynthetic methane seeps and surrounding sediments as natural laboratories in which to contrast relationships between BEF proxies along with a gradient of trophic resource availability (higher resource methane seep, to lower resource photosynthetically fuelled deep-sea habitats). We determined sediment fauna taxonomic and functional trait biodiversity, and quantified bioturbation potential (BPc), calcification degree, standing stock and density as ecosystem functioning proxies. Relationships were strongly unimodal in chemosynthetic seep habitats, but were undetectable in transitional 'chemotone' habitats and photosynthetically dependent deep-sea habitats. In seep habitats, ecosystem functioning proxies peaked below maximum biodiversity, perhaps suggesting that a small number of specialized species are important in shaping this relationship. This suggests that absolute biodiversity is not a good metric of ecosystem 'value' at methane seeps, and that these deep-sea environments may require special management to maintain ecosystem functioning under human disturbance. We promote further investigation of BEF relationships in non-traditional resource environments and emphasize that deep-sea conservation should consider 'functioning hotspots' alongside biodiversity hotspots.

Deep-sea microbes as tools to refine the rules of innate immune pattern recognition.

The assumption of near-universal bacterial detection by pattern recognition receptors is a foundation of immunology. The limits of this pattern recognition concept, however, remain undefined. As a test of this hypothesis, we determined whether mammalian cells can recognize bacteria that they have never had the natural opportunity to encounter. These bacteria were cultivated from the deep Pacific Ocean, where the genus Moritella was identified as a common constituent of the culturable microbiota. Most deep-sea bacteria contained cell wall lipopolysaccharide (LPS) structures that were expected to be immunostimulatory, and some deep-sea bacteria activated inflammatory responses from mammalian LPS receptors. However, LPS receptors were unable to detect 80% of deep-sea bacteria examined, with LPS acyl chain length being identified as a potential determinant of immunosilence. The inability of immune receptors to detect most bacteria from a different ecosystem suggests that pattern recognition strategies may be defined locally, not globally.

Fungal Communities in Sediments Along a Depth Gradient in the Eastern Tropical Pacific.

Deep waters represent the largest biome on Earth and the largest ecosystem of Costa Rica. Fungi play a fundamental role in global biogeochemical cycling in marine sediments, yet, they remain little explored. We studied fungal diversity and community composition in several marine sediments from 16 locations sampled along a bathymetric gradient (from a depth of 380 to 3,474 m) in two transects of about 1,500 km length in the Eastern Tropical Pacific (ETP) of Costa Rica. Sequence analysis of the V7-V8 region of the 18S rRNA gene obtained from sediment cores revealed the presence of 787 fungal amplicon sequence variants (ASVs). On average, we detected a richness of 75 fungal ASVs per sample. Ascomycota represented the most abundant phylum with Saccharomycetes constituting the dominant class. Three ASVs accounted for ca. 63% of all fungal sequences: the yeast Metschnikowia (49.4%), Rhizophydium (6.9%), and Cladosporium (6.7%). We distinguished a cluster composed mainly by yeasts, and a second cluster by filamentous fungi, but we were unable to detect a strong effect of depth and the overlying water temperature, salinity, dissolved oxygen (DO), and pH on the composition of fungal communities. We highlight the need to understand further the ecological role of fungi in deep-sea ecosystems.

Distribution of deep-water scleractinian and stylasterid corals across abiotic environmental gradients on three seamounts in the Anegada Passage.

In the Caribbean Basin the distribution and diversity patterns of deep-sea scleractinian corals and stylasterid hydrocorals are poorly known compared to their shallow-water relatives. In this study, we examined species distribution and community assembly patterns of scleractinian and stylasterid corals on three high-profile seamounts within the Anegada Passage, a deep-water throughway linking the Caribbean Sea and western North Atlantic. Using remotely operated vehicle surveys conducted on the E/V Nautilus by the ROV Hercules in 2014, we characterized coral assemblages and seawater environmental variables between 162 and 2,157 m on Dog Seamount, Conrad Seamount, and Noroît Seamount. In all, 13 morphospecies of scleractinian and stylasterid corals were identified from video with stylasterids being numerically more abundant than both colonial and solitary scleractinians. Cosmopolitan framework-forming species including Madrepora oculata and Solenosmilia variabilis were present but occurred in patchy distributions among the three seamounts. Framework-forming species occurred at or above the depth of the aragonite saturation horizon with stylasterid hydrocorals being the only coral taxon observed below Ωarag values of 1. Coral assemblage variation was found to be strongly associated with depth and aragonite saturation state, while other environmental variables exerted less influence. This study enhances our understanding of the factors that regulate scleractinian and stylasterid coral distribution in an underreported marginal sea and establishes a baseline for monitoring future environmental changes due to ocean acidification and deoxygenation in the tropical western Atlantic.

Methanotrophic bacterial symbionts fuel dense populations of deep-sea feather duster worms (Sabellida, Annelida) and extend the spatial influence of methane seepage.

Deep-sea cold seeps are dynamic sources of methane release and unique habitats supporting ocean biodiversity and productivity. Here, we describe newly discovered animal-bacterial symbioses fueled by methane, between two species of annelid (a serpulid Laminatubus and sabellid Bispira) and distinct aerobic methane-oxidizing bacteria belonging to the Methylococcales, localized to the host respiratory crown. Worm tissue δ13C of -44 to -58‰ are consistent with methane-fueled nutrition for both species, and shipboard stable isotope labeling experiments revealed active assimilation of 13C-labeled methane into animal biomass, which occurs via the engulfment of methanotrophic bacteria across the crown epidermal surface. These worms represent a new addition to the few animals known to intimately associate with methane-oxidizing bacteria and may further explain their enigmatic mass occurrence at 150-million year-old fossil seeps. High-resolution seafloor surveys document significant coverage by these symbioses, beyond typical obligate seep fauna. These findings uncover novel consumers of methane in the deep sea and, by expanding the known spatial extent of methane seeps, may have important implications for deep-sea conservation.

Regulation of ion transport and energy metabolism enables certain coral genotypes to maintain calcification under experimental ocean acidification.

Cold-water corals (CWCs) are important foundation species in the world's largest ecosystem, the deep sea. They support a rich faunal diversity but are threatened by climate change and increased ocean acidification. As part of this study, fragments from three genetically distinct Lophelia pertusa colonies were subjected to ambient pH (pH = 7.9) and low pH (pH = 7.6) for six months. RNA was sampled at two, 4.5, and 8.5 weeks and sequenced. The colony from which the fragments were sampled explained most of the variance in expression patterns, but a general pattern emerged where upregulation of ion transport, required to maintain normal function and calcification, was coincident with lowered expression of genes involved in metabolic processes; RNA regulation and processing in particular. Furthermore, there was no differential expression of carbonic anhydrase detected in any analyses, which agrees with a previously described lack of response in enzyme activity in the same corals. However, one colony was able to maintain calcification longer than the other colonies when exposed to low pH and showed increased expression of ion transport genes including proton transport and expression of genes associated with formation of microtubules and the organic matrix, suggesting that certain genotypes may be better equipped to cope with ocean acidification in the future. While these genotypes exist in the contemporary gene pool, further stresses would reduce the genetic variability of the species, which would have repercussions for the maintenance of existing populations and the ecosystem as a whole.

Climate-induced changes in the suitable habitat of cold-water corals and commercially important deep-sea fishes in the North Atlantic.

The deep sea plays a critical role in global climate regulation through uptake and storage of heat and carbon dioxide. However, this regulating service causes warming, acidification and deoxygenation of deep waters, leading to decreased food availability at the seafloor. These changes and their projections are likely to affect productivity, biodiversity and distributions of deep-sea fauna, thereby compromising key ecosystem services. Understanding how climate change can lead to shifts in deep-sea species distributions is critically important in developing management measures. We used environmental niche modelling along with the best available species occurrence data and environmental parameters to model habitat suitability for key cold-water coral and commercially important deep-sea fish species under present-day (1951-2000) environmental conditions and to project changes under severe, high emissions future (2081-2100) climate projections (RCP8.5 scenario) for the North Atlantic Ocean. Our models projected a decrease of 28%-100% in suitable habitat for cold-water corals and a shift in suitable habitat for deep-sea fishes of 2.0°-9.9° towards higher latitudes. The largest reductions in suitable habitat were projected for the scleractinian coral Lophelia pertusa and the octocoral Paragorgia arborea, with declines of at least 79% and 99% respectively. We projected the expansion of suitable habitat by 2100 only for the fishes Helicolenus dactylopterus and Sebastes mentella (20%-30%), mostly through northern latitudinal range expansion. Our results projected limited climate refugia locations in the North Atlantic by 2100 for scleractinian corals (30%-42% of present-day suitable habitat), even smaller refugia locations for the octocorals Acanella arbuscula and Acanthogorgia armata (6%-14%), and almost no refugia for P. arborea. Our results emphasize the need to understand how anticipated climate change will affect the distribution of deep-sea species including commercially important fishes and foundation species, and highlight the importance of identifying and preserving climate refugia for a range of area-based planning and management tools.

Cold-water coral (Lophelia pertusa) response to multiple stressors: High temperature affects recovery from short-term pollution exposure.

There are numerous studies highlighting the impacts of direct and indirect stressors on marine organisms, and multi-stressor studies of their combined effects are an increasing focus of experimental work. Lophelia pertusa is a framework-forming cold-water coral that supports numerous ecosystem services in the deep ocean. These corals are threatened by increasing anthropogenic impacts to the deep-sea, such as global ocean change and hydrocarbon extraction. This study implemented two sets of experiments to assess the effects of future conditions (temperature: 8 °C and 12 °C, pH: 7.9 and 7.6) and hydrocarbon exposure (oil, dispersant, oil + dispersant combined) on coral health. Phenotypic response was assessed through three independent observations of diagnostic characteristics that were combined into an average health rating at four points during exposure and recovery. In both experiments, regardless of environmental condition, average health significantly declined during 24-hour exposure to dispersant alone but was not significantly altered in the other treatments. In the early recovery stage (24 hours), polyp health returned to the pre-exposure health state under ambient temperature in all treatments. However, increased temperature resulted in a delay in recovery (72 hours) from dispersant exposure. These experiments provide evidence that global ocean change can affect the resilience of corals to environmental stressors and that exposure to chemical dispersants may pose a greater threat than oil itself.

New records of Swiftia (Cnidaria, Anthozoa, Octocorallia) from off the Pacific Costa Rican margin, including a new species from methane seeps.

Exploration of the deep sea off the Pacific margin of Costa Rica has resulted in the discovery of a number of new species and reports for the region. Here, we report on the occurrence of the octocoral genus Swiftia, and describe a new species collected by the Alvin submersible off the Pacific coast of Costa Rica. The new species has been observed at around 1000 m depth, growing on authigenic carbonates near methane seeps. Swiftia sahlingi sp. nov. is characterised by having bright red colonies that are with limited branching, with slightly raised polyp-mounds, thin coenenchyme mainly composed of long warty spindles, and conspicuous plates. A molecular phylogenetic analysis supports the differences between this new taxon and the closest Swiftia species. The new species represents the first record of the genus from Costa Rica and in fact for the Eastern Tropical Pacific.

Growth and feeding of deep-sea coral Lophelia pertusa from the California margin under simulated ocean acidification conditions.

The global decrease in seawater pH known as ocean acidification has important ecological consequences and is an imminent threat for numerous marine organisms. Even though the deep sea is generally considered to be a stable environment, it can be dynamic and vulnerable to anthropogenic disturbances including increasing temperature, deoxygenation, ocean acidification and pollution. Lophelia pertusa is among the better-studied cold-water corals but was only recently documented along the US West Coast, growing in acidified conditions. In the present study, coral fragments were collected at ∼300 m depth along the southern California margin and kept in recirculating tanks simulating conditions normally found in the natural environment for this species. At the collection site, waters exhibited persistently low pH and aragonite saturation states (Ωarag) with average values for pH of 7.66 ± 0.01 and Ωarag of 0.81 ± 0.07. In the laboratory, fragments were grown for three weeks in "favorable" pH/Ωarag of 7.9/1.47 (aragonite saturated) and "unfavorable" pH/Ωarag of 7.6/0.84 (aragonite undersaturated) conditions. There was a highly significant treatment effect (P < 0.001) with an average% net calcification for favorable conditions of 0.023 ± 0.009% d-1 and net dissolution of -0.010 ± 0.014% d-1 for unfavorable conditions. We did not find any treatment effect on feeding rates, which suggests that corals did not depress feeding in low pH/ Ωarag in an attempt to conserve energy. However, these results suggest that the suboptimal conditions for L. pertusa from the California margin could potentially threaten the persistence of this cold-water coral with negative consequences for the future stability of this already fragile ecosystem.