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.

Gene expression profiling reveals deep-sea coral response to the Deepwater Horizon oil spill.

Deep-sea coral communities are key components of the Gulf of Mexico ecosystem and were adversely affected by the Deepwater Horizon (DWH) oil spill. Coral colonies exposed to oil and dispersant exhibited mortality, damage and physiological signatures of stress. Understanding how corals respond to oil and dispersant exposure at the molecular level is important to elucidate the sublethal effects of the DWH disaster and reveal broader patterns of coral stress responses. Gene expression profiles from RNAseq data were compared between corals at an impacted site and from a reference site. A total of 1,439 differentially expressed genes (≥twofold) were shared among impacted Paramuricea biscaya colonies. Genes involved in oxidative stress, immunity, wound repair, tissue regeneration and metabolism of xenobiotics were significantly differentially expressed in impacted corals. Enrichment among the overexpressed genes indicates the corals were enduring high metabolic demands associated with cellular stress responses and repair mechanisms. Underexpression of genes vital to toxin processing also suggests a diminished capacity to cope with environmental stressors. Our results provide evidence that deep-sea corals exhibited genome-wide cellular stress responses to oil and dispersant exposure and demonstrate the utility of next-generation sequencing for monitoring anthropogenic impacts in deep waters. These analyses will facilitate the development of diagnostic markers for oil and dispersant exposure in deep-sea invertebrates and inform future oil spill response efforts.

Extreme longevity in a deep-sea vestimentiferan tubeworm and its implications for the evolution of life history strategies.

The deep sea is home to many species that have longer life spans than their shallow-water counterparts. This trend is primarily related to the decline in metabolic rates with temperature as depth increases. However, at bathyal depths, the cold-seep vestimentiferan tubeworm species Lamellibrachia luymesi and Seepiophila jonesi reach extremely old ages beyond what is predicted by the simple scaling of life span with body size and temperature. Here, we use individual-based models based on in situ growth rates to show that another species of cold-seep tubeworm found in the Gulf of Mexico, Escarpia laminata, also has an extraordinarily long life span, regularly achieving ages of 100-200 years with some individuals older than 300 years. The distribution of results from individual simulations as well as whole population simulations involving mortality and recruitment rates support these age estimates. The low 0.67% mortality rate measurements from collected populations of E. laminata are similar to mortality rates in L. luymesi and S. jonesi and play a role in evolution of the long life span of cold-seep tubeworms. These results support longevity theory, which states that in the absence of extrinsic mortality threats, natural selection will select for individuals that senesce slower and reproduce continually into their old age.

Environmental filtering and neutral processes shape octocoral community assembly in the deep sea.

The ecological and evolutionary processes that interact to shape community structure are poorly studied in the largest environment on earth, the deep sea. Phylogenetic data and morphological traits of octocorals were coupled with environmental factors to test hypotheses of community assembly in the deep (250-2500 m) Gulf of Mexico. We found lineage turnover at a depth of 800-1200 m, with isidids and chrysogorgiids at deeper depths and a diversity of species from across the phylogeny occupying shallower depths. Traits, including axis type, polyp shape, and polyp retraction, differed among species occupying the shallowest (250-800 m) and deepest (1200-2500 m) depths. Results also indicated that octocoral species sort along an environmental gradient of depth. Closely related octocoral species sorted into different depth strata on the upper to middle slope, likely due to barriers imposed by water masses followed by adaptive divergence. Within any given depth zone down to 2000 m, the phylogenetic relatedness of co-existing octocorals was random, indicating that stochastic processes, such as recruitment, also shape community structure. At depths >2000 m, octocorals were more closely related than expected by chance due to the diversification of chrysogorgiids and isidids, which retain conserved traits that impart survival at deeper and/or colder depths. Polyp density, size, and inter-polyp distance were significantly correlated with depth, particularly in plexaurids and isidids, highlighting trait lability across depth and supporting that environmental gradients influence octocoral morphology. Our community phylogenetics approach indicates that both environmental filtering and neutral processes shape community assembly in the deep sea.

Footprint of Deepwater Horizon blowout impact to deep-water coral communities.

On April 20, 2010, the Deepwater Horizon (DWH) blowout occurred, releasing more oil than any accidental spill in history. Oil release continued for 87 d and much of the oil and gas remained in, or returned to, the deep sea. A coral community significantly impacted by the spill was discovered in late 2010 at 1,370 m depth. Here we describe the discovery of five previously unknown coral communities near the Macondo wellhead and show that at least two additional coral communities were impacted by the spill. Although the oil-containing flocullent material that was present on corals when the first impacted community was discovered was largely gone, a characteristic patchy covering of hydrozoans on dead portions of the skeleton allowed recognition of impacted colonies at the more recently discovered sites. One of these communities was 6 km south of the Macondo wellhead and over 90% of the corals present showed the characteristic signs of recent impact. The other community, 22 km southeast of the wellhead between 1,850 and 1,950 m depth, was more lightly impacted. However, the discovery of this site considerably extends the distance from Macondo and depth range of significant impact to benthic macrofaunal communities. We also show that most known deep-water coral communities in the Gulf of Mexico do not appear to have been acutely impacted by the spill, although two of the newly discovered communities near the wellhead apparently not impacted by the spill have been impacted by deep-sea fishing operations.

Testing the depth-differentiation hypothesis in a deepwater octocoral.

The depth-differentiation hypothesis proposes that the bathyal region is a source of genetic diversity and an area where there is a high rate of species formation. Genetic differentiation should thus occur over relatively small vertical distances, particularly along the upper continental slope (200-1000 m) where oceanography varies greatly over small differences in depth. To test whether genetic differentiation within deepwater octocorals is greater over vertical rather than geographical distances, Callogorgia delta was targeted. This species commonly occurs throughout the northern Gulf of Mexico at depths ranging from 400 to 900 m. We found significant genetic differentiation (FST = 0.042) across seven sites spanning 400 km of distance and 400 m of depth. A pattern of isolation by depth emerged, but geographical distance between sites may further limit gene flow. Water mass boundaries may serve to isolate populations across depth; however, adaptive divergence with depth is also a possible scenario. Microsatellite markers also revealed significant genetic differentiation (FST = 0.434) between C. delta and a closely related species, Callogorgia americana, demonstrating the utility of microsatellites in species delimitation of octocorals. Results provided support for the depth-differentiation hypothesis, strengthening the notion that factors covarying with depth serve as isolation mechanisms in deep-sea populations.

Impact of the Deepwater Horizon oil spill on a deep-water coral community in the Gulf of Mexico.

To assess the potential impact of the Deepwater Horizon oil spill on offshore ecosystems, 11 sites hosting deep-water coral communities were examined 3 to 4 mo after the well was capped. Healthy coral communities were observed at all sites >20 km from the Macondo well, including seven sites previously visited in September 2009, where the corals and communities appeared unchanged. However, at one site 11 km southwest of the Macondo well, coral colonies presented widespread signs of stress, including varying degrees of tissue loss, sclerite enlargement, excess mucous production, bleached commensal ophiuroids, and covering by brown flocculent material (floc). On the basis of these criteria the level of impact to individual colonies was ranked from 0 (least impact) to 4 (greatest impact). Of the 43 corals imaged at that site, 46% exhibited evidence of impact on more than half of the colony, whereas nearly a quarter of all of the corals showed impact to >90% of the colony. Additionally, 53% of these corals' ophiuroid associates displayed abnormal color and/or attachment posture. Analysis of hopanoid petroleum biomarkers isolated from the floc provides strong evidence that this material contained oil from the Macondo well. The presence of recently damaged and deceased corals beneath the path of a previously documented plume emanating from the Macondo well provides compelling evidence that the oil impacted deep-water ecosystems. Our findings underscore the unprecedented nature of the spill in terms of its magnitude, release at depth, and impact to deep-water ecosystems.

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.

Niche divergence by deep-sea octocorals in the genus Callogorgia across the continental slope of the Gulf of Mexico.

Environmental variables that are correlated with depth have been suggested to be among the major forces underlying speciation in the deep sea. This study incorporated phylogenetics and ecological niche models (ENM) to examine whether congeneric species of Callogorgia (Octocorallia: Primnoidae) occupy different ecological niches across the continental slope of the Gulf of Mexico (GoM) and whether this niche divergence could be important in the evolution of these closely related species. Callogorgia americana americana, Callogorgia americana delta and Callogorgia gracilis were documented at 13 sites in the GoM (250-1000 m) from specimen collections and extensive video observations. On a first order, these species were separated by depth, with C. gracilis occurring at the shallowest sites, C. a. americana at mid-depths and C. a. delta at the deepest sites. Callogorgia a. delta was associated with areas of increased seep activity, whereas C. gracilis and C. a. americana were associated with narrow, yet warmer, temperature ranges and did not occur near cold seeps. ENM background and identity tests revealed little to no overlap in ecological niches between species. Temporal calibration of the phylogeny revealed the formation of the Isthmus of Panama was a vicariance event that may explain some of the patterns of speciation within this genus. These results elucidate the potential mechanisms for speciation in the deep sea, emphasizing both bathymetric speciation and vicariance events in the evolution of a genus across multiple regions.

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.

Deep-sea impacts of climate interventions.

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

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.

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.

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.

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.

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.