The Mitogenomic Landscape of Hexacorallia Corals: Insight into Their Slow Evolution.

The utility of the mitochondrial genomes (mitogenomes) in analyzing the evolutionary history of animals has been proven. Five deep-sea corals (Bathypathes sp.1, Bathypathes sp.2, Schizopathidae 1, Trissopathes sp., and Leiopathes sp.) were collected in the South China Sea (SCS). Initially, the structures and collinearity of the five deep-sea coral mitogenomes were analyzed. The gene arrangements in the five deep-sea coral mitogenomes were similar to those in the order Antipatharia, which evidenced their conservation throughout evolutionary history. Additionally, to elucidate the slow evolutionary rates in Hexacorallia mitogenomes, we conducted comprehensive analyses, including examining phylogenetic relationships, performing average nucleotide identity (ANI) analysis, and assessing GC-skew dissimilarity combining five deep-sea coral mitogenomes and 522 reference Hexacorallia mitogenomes. Phylogenetic analysis using 13 conserved proteins revealed that species clustered together at the order level, and they exhibited interspersed distributions at the family level. The ANI results revealed that species had significant similarities (identity > 85%) within the same order, while species from different orders showed notable differences (identity < 80%). The investigation of the Hexacorallia mitogenomes also highlighted that the GC-skew dissimilarity was highly significant at the order level, but not as pronounced at the family level. These results might be attributed to the slow evolution rate of Hexacorallia mitogenomes and provide evidence of mitogenomic diversity. Furthermore, divergence time analysis revealed older divergence times assessed via mitogenomes compared with nuclear data, shedding light on significant evolutionary events shaping distinct orders within Hexacorallia corals. Those findings provide new insights into understanding the slow evolutionary rates of deep-sea corals in all lineages of Hexacorallia using their mitogenomes.

Transcriptome assemblies of two deep-sea octocorals Calyptrophora lyra and Chrysogorgia stellata from West Pacific seamount, Godin Guyot.

This is the first report of the transcriptome assemblies of the deep-sea octocorals Calyptrophora lyra and Chrysogorgia stellata, which were collected in a survey of the West Pacific seamounts area. We sequenced the transcriptomes of C. lyra and C. stellata using the Illumina NovaSeq 6000 System. De novo assembly and analysis of the coding regions predicted 193,796 unigenes from the total 116,441,796 reads of C. lyra and 235,513 unigenes from the total 122,031,866 reads of C. stellata. Our data are a valuable resource with which to understand the ecological and biological characteristics of the West Pacific deep-sea corals. The data will also contribute to the study of deep-sea environments as extreme and limited habitats and provide direction for future research and further insight into the organismal responses of deep-sea corals to environmental changes.

Vulnerability of six cold-water corals to sediment resuspension from bottom trawling fishing.

Bottom trawling can significantly affect benthic communities, directly through immediate removal of sessile organisms and indirectly through sediment resuspension. Submarine canyons, often surrounded by fishing grounds, are important habitats for cold-water corals (CWC). Vulnerability of CWCs to increased suspended sediment concentration (SSC) is key to understanding the severity of bottom trawling effects on those communities. Here we show survival, growth, and physiological response of six CWCs from a Mediterranean submarine canyon (Dendrophyllia cornigera, Desmophyllum dianthus, Desmophyllum pertusum, Madrepora oculata, Leiopathes glaberrima and Muriceides lepida), exposed to a long-term, aquarium-based sedimentary disturbance experiment. Compared to cup coral and octocoral, which did not exhibit symptoms of distress, our data indicate that colonial scleractinian corals and black coral, which experienced substantial polyp mortality in enhanced SSC treatments, are more vulnerable. Indirect impact of bottom trawling could thus contribute to structural simplification of CWC communities posing an additional stressor alongside with global climate change.

Microbial Associations of Abyssal Gorgonians and Anemones (>4,000 m Depth) at the Clarion-Clipperton Fracture Zone.

Deep coral-dominated communities play paramount roles in benthic environments by increasing their complexity and biodiversity. Coral-associated microbes are crucial to maintain fitness and homeostasis at the holobiont level. However, deep-sea coral biology and their associated microbiomes remain largely understudied, and less from remote and abyssal environments such as those in the Clarion-Clipperton Fracture Zone (CCZ) in the tropical Northeast (NE) Pacific Ocean. Here, we study microbial-associated communities of abyssal gorgonian corals and anemones (>4,000 m depth) in the CCZ; an area harboring the largest known global reserve of polymetallic nodules that are commercially interesting for the deep-sea nodule mining. Coral samples (n = 25) belonged to Isididae and Primnoidae families, while anemones (n = 4) to Actinostolidae family. Significant differences in bacterial community compositions were obtained between these three families, despite sharing similar habitats. Anemones harbored bacterial microbiomes composed mainly of Hyphomicrobiaceae, Parvibaculales, and Pelagibius members. Core microbiomes of corals were mainly dominated by different Spongiibacteraceae and Terasakiellaceae bacterial members, depending on corals' taxonomy. Moreover, the predicted functional profiling suggests that deep-sea corals harbor bacterial communities that allow obtaining additional energy due to the scarce availability of nutrients. This study presents the first report of microbiomes associated with abyssal gorgonians and anemones and will serve as baseline data and crucial insights to evaluate and provide guidance on the impacts of deep-sea mining on these key abyssal communities.

Description of a new and widely distributed species of Bathypathes (Cnidaria: Anthozoa: Antipatharia: Schizopathidae) previously misidentified as Bathypathes alternata Brook, 1889.

For many years an undescribed species of the genus Bathypathes has been misidentified as Bathypathes alternata Brook, 1889 (a species currently re-assigned to the genus Alternatipathes). This new species is rather common at mid- and lower bathyal depths of the Pacific, Atlantic and Indian oceans, often in areas with high concentrations of commercially valuable cobalt-rich ferromanganese crusts, where it was observed in underwater photo and video transects to occur in high densities. Under the name B. alternata this species is recorded in several inventories and databases. There is an urgent need for a formal description of this misidentified and widely distributed species to avoid further confusion. The new species is superficially similar to A. alternata in having a monopodial corallum and simple, bilateral and alternately arranged pinnules. However, it differs from the former in that it has an upright corallum with a straight pinnulated part (vs. a horizontally bent pinnulated part), pinnules of uniform length and density (vs. decreasing regularly distally), and a constant distal angle formed by the pinnules and the stem along different parts of the corallum (vs. a decreasing distal angle near the top). The new species can therefore be easily distinguished from A. alternata in underwater imagery. We formally describe this new species in the genus Bathypathes and assign it the new name B. pseudoalternata. An extensive synonymy list with previous misidentified records is provided. To evaluate the distributional patterns of the new species we review the geographic distribution of antipatharians reported below 800 m. The majority of the hitherto described lower bathyal and abyssal species have been recorded from one biogeographic province; however, 20 species are known from more than two provinces, and only three species are widely distributed (>5 provinces), including the newly described Bathypathes pseudoalternata. Members of the family Schizopathidae, to which the new species belongs, represent the majority of the lower bathyal (50.54%) and abyssal (82.35%) species.

The carbon and nitrogen budget of Desmophyllum dianthus-a voracious cold-water coral thriving in an acidified Patagonian fjord.

In the North Patagonian fjord region, the cold-water coral (CWC) Desmophyllum dianthus occurs in high densities, in spite of low pH and aragonite saturation. If and how these conditions affect the energy demand of the corals is so far unknown. In a laboratory experiment, we investigated the carbon and nitrogen (C, N) budget of D. dianthus from Comau Fjord under three feeding scenarios: (1) live fjord zooplankton (100-2,300 µm), (2) live fjord zooplankton plus krill (>7 mm), and (3) four-day food deprivation. In closed incubations, C and N budgets were derived from the difference between C and N uptake during feeding and subsequent C and N loss through respiration, ammonium excretion, release of particulate organic carbon and nitrogen (POC, PON). Additional feeding with krill significantly increased coral respiration (35%), excretion (131%), and POC release (67%) compared to feeding on zooplankton only. Nevertheless, the higher C and N losses were overcompensated by the threefold higher C and N uptake, indicating a high assimilation and growth efficiency for the krill plus zooplankton diet. In contrast, short food deprivation caused a substantial reduction in respiration (59%), excretion (54%), release of POC (73%) and PON (87%) compared to feeding on zooplankton, suggesting a high potential to acclimatize to food scarcity (e.g., in winter). Notwithstanding, unfed corals 'lost' 2% of their tissue-C and 1.2% of their tissue-N per day in terms of metabolism and released particulate organic matter (likely mucus). To balance the C (N) losses, each D. dianthus polyp has to consume around 700 (400) zooplankters per day. The capture of a single, large krill individual, however, provides enough C and N to compensate daily C and N losses and grow tissue reserves, suggesting that krill plays an important nutritional role for the fjord corals. Efficient krill and zooplankton capture, as well as dietary and metabolic flexibility, may enable D. dianthus to thrive under adverse environmental conditions in its fjord habitat; however, it is not known how combined anthropogenic warming, acidification and eutrophication jeopardize the energy balance of this important habitat-building species.

Effects of low pH and feeding on calcification rates of the cold-water coral Desmophyllum dianthus.

Cold-Water Corals (CWCs), and most marine calcifiers, are especially threatened by ocean acidification (OA) and the decrease in the carbonate saturation state of seawater. The vulnerability of these organisms, however, also involves other global stressors like warming, deoxygenation or changes in sea surface productivity and, hence, food supply via the downward transport of organic matter to the deep ocean. This study examined the response of the CWC Desmophyllum dianthus to low pH under different feeding regimes through a long-term incubation experiment. For this experiment, 152 polyps were incubated at pH 8.1, 7.8, 7.5 and 7.2 and two feeding regimes for 14 months. Mean calcification rates over the entire duration of the experiment ranged between -0.3 and 0.3 mg CaCO3 g-1d-1. Polyps incubated at pH 7.2 were the most affected and 30% mortality was observed in this treatment. In addition, many of the surviving polyps at pH 7.2 showed negative calcification rates indicating that, in the long term, CWCs may have difficulty thriving in such aragonite undersaturated waters. The feeding regime had a significant effect on skeletal growth of corals, with high feeding frequency resulting in more positive and variable calcification rates. This was especially evident in corals reared at pH 7.5 (ΩA = 0.8) compared to the low frequency feeding treatment. Early life-stages, which are essential for the recruitment and maintenance of coral communities and their associated biodiversity, were revealed to be at highest risk. Overall, this study demonstrates the vulnerability of D. dianthus corals to low pH and low food availability. Future projected pH decreases and related changes in zooplankton communities may potentially compromise the viability of CWC populations.

Uptake and distribution of organo-iodine in deep-sea corals.

Understanding iodine concentration, transport, and bioavailability is essential in evaluating iodine's impact to the environment and its effectiveness as an environmental biogeotracer. While iodine and its radionuclides have proven to be important tracers in geologic and biologic studies, little is known about transport of this element to the deep sea and subsequent uptake in deep-sea coral habitats. Results presented here on deep-sea black coral iodine speciation and iodine isotope variability provides key information on iodine behavior in natural and anthropogenic environments, and its geochemical pathway in the Gulf of Mexico. Organo-iodine is the dominant iodine species in the black corals, demonstrating that binding of iodine to organic matter plays an important role in the transport and transfer of iodine to the deep-sea corals. The identification of growth bands captured in high-resolution scanning electron images (SEM) with synchronous peaks in iodine variability suggest that riverine delivery of terrestrial-derived organo-iodine is the most plausible explanation to account for annual periodicity in the deep-sea coral geochemistry. Whereas previous studies have suggested the presence of annual growth rings in deep-sea corals, this present study provides a mechanism to explain the formation of annual growth bands. Furthermore, deep-sea coral ages based on iodine peak counts agree well with those ages derived from radiocarbon (14C) measurements. These results hold promise for developing chronologies independent of 14C dating, which is an essential component in constraining reservoir ages and using radiocarbon as a tracer of ocean circulation. Furthermore, the presence of enriched 129I/127I ratios during the most recent period of skeleton growth is linked to nuclear weapons testing during the 1960s. The sensitivity of the coral skeleton to record changes in surface water 129I composition provides further evidence that iodine composition and isotope variability captured in proteinaceous deep-sea corals is a promising geochronometer as well as an emerging tracer for continental material flux.

The physiological response of the deep-sea coral Solenosmilia variabilis to ocean acidification.

Several forms of calcifying scleractinian corals provide important habitat complexity in the deep-sea and are consistently associated with a high biodiversity of fish and other invertebrates. How these corals may respond to the future predicted environmental conditions of ocean acidification is poorly understood, but any detrimental effects on these marine calcifiers will have wider impacts on the ecosystem. Colonies of Solenosmilia variabilis, a protected deep-sea coral commonly occurring throughout the New Zealand region, were collected during a cruise in March 2014 from the Louisville Seamount Chain. Over a 12-month period, samples were maintained in temperature controlled (∼3.5 °C) continuous flow-through tanks at a seawater pH that reflects the region's current conditions (7.88) and an end-of-century scenario (7.65). Impacts on coral growth and the intensity of colour saturation (as a proxy for the coenenchyme tissue that covers the coral exoskeleton and links the coral polyps) were measured bimonthly. In addition, respiration rate was measured after a mid-term (six months) and long-term (12 months) exposure period. Growth rates were highly variable, ranging from 0.53 to 3.068 mm year-1 and showed no detectable difference between the treatment and control colonies. Respiration rates also varied independently of pH and ranged from 0.065 to 1.756 µmol O2 g protein-1 h-1. A significant change in colour was observed in the treatment group over time, indicating a loss of coenenchyme. This loss was greatest after 10 months at 5.28% and could indicate a reallocation of energy with physiological processes (e.g.  growth and respiration) being maintained at the expense of coenenchyme production. This research illustrates important first steps to assessing and understanding the sensitivity of deep-sea corals to ocean acidification.

Biogeographic Comparison of Lophelia-Associated Bacterial Communities in the Western Atlantic Reveals Conserved Core Microbiome.

Over the last decade, publications on deep-sea corals have tripled. Most attention has been paid to Lophelia pertusa, a globally distributed scleractinian coral that creates critical three-dimensional habitat in the deep ocean. The bacterial community associated with L. pertusa has been previously described by a number of studies at sites in the Mediterranean Sea, Norwegian fjords, off Great Britain, and in the Gulf of Mexico (GOM). However, use of different methodologies prevents direct comparisons in most cases. Our objectives were to address intra-regional variation and to identify any conserved bacterial core community. We collected samples from three distinct colonies of L. pertusa at each of four locations within the western Atlantic: three sites within the GOM and one off the east coast of the United States. Amplicon libraries of 16S rRNA genes were generated using primers targeting the V4-V5 hypervariable region and 454 pyrosequencing. The dominant phylum was Proteobacteria (75-96%). At the family level, 80-95% of each sample was comprised of five groups: Pirellulaceae, Pseudonocardiaceae, Rhodobacteraceae, Sphingomonadaceae, and unclassified Oceanospirillales. Principal coordinate analysis based on weighted UniFrac distances showed a clear distinction between the GOM and Atlantic samples. Interestingly, the replicate samples from each location did not always cluster together, indicating there is not a strong site-specific influence. The core bacterial community, conserved in 100% of the samples, was dominated by the operational taxonomic units of genera Novosphingobium and Pseudonocardia, both known degraders of aromatic hydrocarbons. The sequence of another core member, Propionibacterium, was also found in prior studies of L. pertusa from Norway and Great Britain, suggesting a role as a conserved symbiont. By examining more than 40,000 sequences per sample, we found that GOM samples were dominated by the identified conserved core sequences, whereas open Atlantic samples had a much higher proportion of locally consistent bacteria. Further, predictive functional profiling highlights the potential for the L. pertusa microbiome to contribute to chemoautotrophy, nutrient cycling, and antibiotic production.

Octocoral mitochondrial genomes provide insights into the phylogenetic history of gene order rearrangements, order reversals, and cnidarian phylogenetics.

We use full mitochondrial genomes to test the robustness of the phylogeny of the Octocorallia, to determine the evolutionary pathway for the five known mitochondrial gene rearrangements in octocorals, and to test the suitability of using mitochondrial genomes for higher taxonomic-level phylogenetic reconstructions. Our phylogeny supports three major divisions within the Octocorallia and show that Paragorgiidae is paraphyletic, with Sibogagorgia forming a sister branch to the Coralliidae. Furthermore, Sibogagorgia cauliflora has what is presumed to be the ancestral gene order in octocorals, but the presence of a pair of inverted repeat sequences suggest that this gene order was not conserved but rather evolved back to this apparent ancestral state. Based on this we recommend the resurrection of the family Sibogagorgiidae to fix the paraphyly of the Paragorgiidae. This is the first study to show that in the Octocorallia, mitochondrial gene orders have evolved back to an ancestral state after going through a gene rearrangement, with at least one of the gene orders evolving independently in different lineages. A number of studies have used gene boundaries to determine the type of mitochondrial gene arrangement present. However, our findings suggest that this method known as gene junction screening may miss evolutionary reversals. Additionally, substitution saturation analysis demonstrates that while whole mitochondrial genomes can be used effectively for phylogenetic analyses within Octocorallia, their utility at higher taxonomic levels within Cnidaria is inadequate. Therefore for phylogenetic reconstruction at taxonomic levels higher than subclass within the Cnidaria, nuclear genes will be required, even when whole mitochondrial genomes are available.

A pesca demersal de profundidade e os bancos de corais azooxantelados do sul do Brasil / The deep-sea demersal fisheries and the azooxanthellate corals from southern Brazil

A pesca demersal voltada as espécies de peixes (i.e. Lophius gastrophisus, Urophisys brasiliensis, Genipterus brasiliensis) e crustáceos (Chaceon ramosae e Chaceon sp.), com grande valor comercial no talude continental superior do sul do Brasil aumentou significativamente nas últimas décadas. A compilação de todos os dados até então publicados acerca dos pontos de ocorrência dos corais escleractíneos azooxantelados em águas sul-brasileiras entre 24º e 35º S, sobrepostos com as principais áreas de atuação das quatro modalidades de pesca demersais (arrasto de profundidade, emalhe e espinhel de fundo e covos), demonstrou que as frotas em questão vêm utilizando as áreas com ocorrência de corais, como principais áreas de esforço, indicando que os recifes de profundidade possuem elevada importância ecológica perante os ecossistemas da plataforma e talude continental, sendo importantes reservatórios da biodiversidade marinha profunda. Entretanto, desde as fases iniciais desta exploração evidenciou-se através de relatos de observadores de bordo, a captura, como "bycatch", de grandes quantidades de corais de profundidade. Desta maneira, visando não só apenas a proteção dos ecossistemas coralíneos de profundidade, mas também a sustentabilidade econômica da pesca, é recomendada a criação de áreas de exclusão da pesca demersal em locais com ocorrência de Scleractinia azooxantelados.

Demersal fishing of important commercial fishes (Lophius gastrophisus, Urophisys brasiliensis and Genipterus brasiliensis) and crustaceans (Chaceon ramosae and Chaceon sp.) along the upper slope off southern Brazil has increased dramatically in the last decade. Compilation of available data on the distribution of azooxanthellate corals between 24º and 35º S, compared with the distribution of bottom-longline, bottom-gillnets, trawl and trap fisheries shows that commercial fishing takes place over coral areas, providing evidence deep-sea reefs are important reservoirs of deep marine biodiversity. Since the initial phase of exploitation by demersal fisheries, onboard observers are describing large captures of corals as "bycatch" suggesting deep-sea communities are being destroyed even before being studied. In order to ensure protection of deep-sea coral ecosystems and economic sustainability of demersal fisheries in southern Brazilian waters, adoption of excluded fishing areas in those locations where azooxanthellate Scleractinia occur is strongly recommended.