Despite the current decline of scleractinian coral populations, octocorals are thriving on reefs in the Caribbean Sea and western North Atlantic Ocean. These cnidarians are holobiont entities, interacting with a diverse array of microorganisms. Few studies have investigated the spatial and temporal stability of the bacterial communities associated with octocoral species and information regarding the co-occurrence and potential interactions between specific members of these bacterial communities remain sparse. To address this knowledge gap, this study investigated the stability of the bacterial assemblages associated with two common Caribbean octocoral species, Eunicea flexuosa and Antillogorgia americana, across time and geographical locations and performed network analyses to investigate potential bacterial interactions. Results demonstrated that general inferences regarding the spatial and temporal stability of octocoral-associated bacterial communities should not be made, as host-specific characteristics may influence these factors. In addition, network analyses revealed differences in the complexity of the interactions between bacteria among the octocoral species analyzed, while highlighting the presence of genera known to produce bioactive secondary metabolites in both octocorals that may play fundamental roles in structuring the octocoral-associated bacteriome.
UNASSIGNED: The online version contains supplementary material available at 10.1007/s13199-023-00923-x.

The role of bacterial symbionts that populate octocorals (Cnidaria, Octocorallia) is still poorly understood. To shed light on their metabolic capacities, we examined 66 high-quality metagenome-assembled genomes (MAGs) spanning 30 prokaryotic species, retrieved from microbial metagenomes of three octocoral species and seawater.
Symbionts of healthy octocorals were affiliated with the taxa Endozoicomonadaceae, Candidatus Thioglobaceae, Metamycoplasmataceae, unclassified Pseudomonadales, Rhodobacteraceae, unclassified Alphaproteobacteria and Ca. Rhabdochlamydiaceae. Phylogenomics inference revealed that the Endozoicomonadaceae symbionts uncovered here represent two species of a novel genus unique to temperate octocorals, here denoted Ca. Gorgonimonas eunicellae and Ca. Gorgonimonas leptogorgiae. Their genomes revealed metabolic capacities to thrive under suboxic conditions and high gene copy numbers of serine-threonine protein kinases, type 3-secretion system, type-4 pili, and ankyrin-repeat proteins, suggesting excellent capabilities to colonize, aggregate, and persist inside their host. Contrarily, MAGs obtained from seawater frequently lacked symbiosis-related genes. All Endozoicomonadaceae symbionts harbored endo-chitinase and chitin-binging protein-encoding genes, indicating that they can hydrolyze the most abundant polysaccharide in the oceans. Other symbionts, including Metamycoplasmataceae and Ca. Thioglobaceae, may assimilate the smaller chitin oligosaccharides resulting from chitin breakdown and engage in chitin deacetylation, respectively, suggesting possibilities for substrate cross-feeding and a role for the coral microbiome in overall chitin turnover. We also observed sharp differences in secondary metabolite production potential between symbiotic lineages. Specific Proteobacteria taxa may specialize in chemical defense and guard other symbionts, including Endozoicomonadaceae, which lack such capacity.
This is the first study to recover MAGs from dominant symbionts of octocorals, including those of so-far unculturable Endozoicomonadaceae, Ca. Thioglobaceae and Metamycoplasmataceae symbionts. We identify a thus-far unanticipated, global role for Endozoicomonadaceae symbionts of corals in the processing of chitin, the most abundant natural polysaccharide in the oceans and major component of the natural zoo- and phytoplankton feed of octocorals. We conclude that niche partitioning, metabolic specialization, and adaptation to low oxygen conditions among prokaryotic symbionts likely contribute to the plasticity and adaptability of the octocoral holobiont in changing marine environments. These findings bear implications not only for our understanding of symbiotic relationships in the marine realm but also for the functioning of benthic ecosystems at large. Video Abstract.

The frequency and severity of marine heatwaves causing mass mortality events in tropical and temperate coral species increases every year, with serious consequences on the stability and resilience of coral populations. Although recovery and persistence of coral populations after stress events is closely related to adult fitness, as well as larval survival and settlement, much remains unknown about the effects of thermal stress on early life-history stages of temperate coral species. In the present study, the reproductive phenology and the effect of increased water temperature (+4°C and +6°C above ambient, 20°C) on larval survival and settlement was evaluated for two of the most representative Mediterranean octocoral species (Eunicella singularis and Corallium rubrum). Our study shows that reproductive behavior is more variable than previously reported and breeding period occurs over a longer period in both species. Thermal stress did not affect the survival of symbiotic E. singularis larvae but drastically reduced the survival of the non-symbiotic C. rubrum larvae. Results on larval biomass and caloric consumption suggest that higher mortality rates of C. rubrum exposed to increased temperature were not related to depletion of endogenous energy in larvae. The results also show that settlement rates of E. singularis did not change in response to elevated temperature after 20 days of exposure, but larvae may settle fast and close to their native population at 26°C (+6°C). Although previous experimental studies found that adult colonies of both octocoral species are mostly resistant to thermal stress, our results on early life-history stages suggest that the persistence and inter-connectivity of local populations may be severely compromised under continued trends in ocean warming.

Understanding the resilience of temperate reefs to climate change requires exploring the recovery capacity of their habitat-forming species from recurrent marine heatwaves (MHWs). Here, we show that, in a Mediterranean highly enforced marine protected area established more than 40 years ago, habitat-forming octocoral populations that were first affected by a severe MHW in 2003 have not recovered after 15 years. Contrarily, they have followed collapse trajectories that have brought them to the brink of local ecological extinction. Since 2003, impacted populations of the red gorgonian Paramuricea clavata (Risso, 1826) and the red coral Corallium rubrum (Linnaeus, 1758) have followed different trends in terms of size structure, but a similar progressive reduction in density and biomass. Concurrently, recurrent MHWs were observed in the area during the 2003-2018 study period, which may have hindered populations recovery. The studied octocorals play a unique habitat-forming role in the coralligenous assemblages (i.e. reefs endemic to the Mediterranean Sea home to approximately 10% of its species). Therefore, our results underpin the great risk that recurrent MHWs pose for the long-term integrity and functioning of these emblematic temperate reefs.

The present study aims at contributing to the knowledge of the spatial variability of coralligenous reefs through the evaluation of patterns ranging from local to biogeographic scale around the island of Sardinia. The coralligenous reef assemblages of six areas were studied through a hierarchical sampling design: three sites per area were selected, in each site three plots were sampled and in each plot ten photographic samples were collected. The structure of coralligenous reefs across closed biogeographic regions is described, highlighting that nearly pristine assemblages, although characterized by similar high diversity, can be either dominated by animals, such as gorgonians and bryozoans, or macroalgae. The observed variations seem largely related to biogeographic patterns rather than spatial distance, supporting the need to identify specific reference conditions to assess the ecological quality of this habitat depending on the biogeographic area to be monitored.

In octocorals (Cnidaria Octocorallia), the functional relationship between host health and its symbiotic consortium has yet to be determined. Here, we employed comparative metagenomics to uncover the distinct functional and phylogenetic features of the microbiomes of healthy Eunicella gazella, Eunicella verrucosa, and Leptogorgia sarmentosa tissues, in contrast with the microbiomes found in seawater and sediments. We further explored how the octocoral microbiome shifts to a pathobiome state in E. gazella.
Multivariate analyses based on 16S rRNA genes, Clusters of Orthologous Groups of proteins (COGs), Protein families (Pfams), and secondary metabolite-biosynthetic gene clusters annotated from 20 Illumina-sequenced metagenomes each revealed separate clustering of the prokaryotic communities of healthy tissue samples of the three octocoral species from those of necrotic E. gazella tissue and surrounding environments. While the healthy octocoral microbiome was distinguished by so-far uncultivated Endozoicomonadaceae, Oceanospirillales, and Alteromonadales phylotypes in all host species, a pronounced increase of Flavobacteriaceae and Alphaproteobacteria, originating from seawater, was observed in necrotic E. gazella tissue. Increased abundances of eukaryotic-like proteins, exonucleases, restriction endonucleases, CRISPR/Cas proteins, and genes encoding for heat-shock proteins, inorganic ion transport, and iron storage distinguished the prokaryotic communities of healthy octocoral tissue regardless of the host species. An increase of arginase and nitric oxide reductase genes, observed in necrotic E. gazella tissues, suggests the existence of a mechanism for suppression of nitrite oxide production by which octocoral pathogens may overcome the host\'s immune system.
This is the first study to employ primer-less, shotgun metagenome sequencing to unveil the taxonomic, functional, and secondary metabolism features of prokaryotic communities in octocorals. Our analyses reveal that the octocoral microbiome is distinct from those of the environmental surroundings, is host genus (but not species) specific, and undergoes large, complex structural changes in the transition to the dysbiotic state. Host-symbiont recognition, abiotic-stress response, micronutrient acquisition, and an antiviral defense arsenal comprising multiple restriction endonucleases, CRISPR/Cas systems, and phage lysogenization regulators are signatures of prokaryotic communities in octocorals. We argue that these features collectively contribute to the stabilization of symbiosis in the octocoral holobiont and constitute beneficial traits that can guide future studies on coral reef conservation and microbiome therapy. Video Abstract.

Three new sea fan species of Leptogorgia were discovered during multiple scuba diving expeditions along the Gulf of California coast and islands. Leptogorgia iridis sp. nov. is distributed in the southern region of the gulf (Mexican Province), inhabiting tropical rocky reefs of the Islas Marías Archipelago (Nayarit) and Bahía Banderas (Jalisco). This species has small colonies (< 7 cm height) with at least five clearly distinct chromotypes. Leptogorgia martirensis sp. nov. was found exclusively on the rocky reefs of San Pedro Mártir and San Esteban Islands located in the northern region of the Gulf of California (northern region of Cortez Province). Leptogorgia enrici sp. nov. is distributed from the south to the northern region of the Gulf of California (Cortez Province), inhabiting substrates of rocky reefs, sandy and pebbly sea floors. Comprehensive ecological diving expeditions to identify and classify octocorals in the Mexican Pacific (1995-2019) indicate that L. iridis sp. nov. and L. martirensis sp. nov. are likely to be micro-endemics and L. enrici sp. nov. is endemic to the Gulf of California, which defines their currently known biogeographic distribution ranges.

Coral reefs throughout the tropics have experienced large declines in the abundance of scleractinian corals over the last few decades, and some reefs are becoming functionally dominated by animal taxa other than scleractinians. This phenomenon is striking on many shallow reefs in the tropical western Atlantic, where arborescent octocorals now are numerically and functionally dominant. Octocorals are one of several taxa that have been overlooked for decades in analyses of coral reef community dynamics, and our understanding of why octocorals are favoured (whereas scleractinians are not) on some modern reefs, and how they will affect the function of future reef communities, is not commensurate with the task of scientifically responding to the coral reef crisis. We summarize the biological and ecological features predisposing octocorals for success under contemporary conditions, and focus on those features that could have generated resistance and resilience of octocoral populations to environmental change on modern reefs. There is a rich set of opportunities for rapid advancement in understanding the factors driving the success of octocorals on modern reefs, but we underscore three lines of inquiry: (1) the functional implications of strongly mixotrophic, polytrophic, and plastic nutrition, (2) the capacity to recruit at high densities and maintain rapid initial rates of vertical growth, and (3) the emergent properties associated with dense animal forests at high colony densities.

Since about the turn of the millennium, octocorals have been increasing in abundance on Caribbean reefs. The mechanisms underlying this trend have not been resolved, but the emergent species assemblage appears to be more resilient than the scleractinians they are replacing. The sea fan Gorgonia ventalina is an iconic species in the contemporary octocoral fauna, and here its population dynamics are described from St. John, US Virgin Islands, from 2013 to 2019. Mean densities of G. ventalina at Yawzi Point (9-m depth) varied from 1.4-1.5 colonies m-2, and their mean heights from 24-30 cm; nearby at Tektite (14-m depth), they varied from 0.6-0.8 colonies m-2 and from 25-33 cm. These reefs were impacted by two Category 5 hurricanes in 2017, but neither the density of G. ventalina, the density of their recruits (< 5-cm tall), nor the height of colonies, differed among years, although growth was depressed after the hurricanes. Nevertheless, at Tektite, colony height trended upwards over time, in part because colonies 10.1-20 cm tall were reduced in abundance after the hurricanes. These trends were sustained without density-associated effects mediating recruitment or self-thinning of adults. The dynamics of G. ventalina over seven years reveals the high resilience of this species that will contribute to the persistence of octocorals as a dominant state on Caribbean reefs.

The species of the genus Psammogorgia Verrill, 1868 from the shallow waters of the tropical eastern Pacific were mainly described from 1846 to 1870. Very few contributions were published subsequently. Recently, the genus was revisited with the addition of two new species. However, a comprehensive generic study is still missing for the eastern Pacific. Psammogorgia is characterised by having axes cores without mineralisation, mainly coarse irregular spindles and thorny, leafy or tuberculate clubs coenenchymal sclerites and the anthocodial armature with distinct collaret and points arrangements. Herein a taxonomic revision of the genus is presented based on type material which was morphologically analysed and illustrated using optical and scanning electron microscopy. Comparative character tables are provided for comparison among species in the genus, along with a taxonomic key. Moreover, the taxonomic status of each species was analysed. The genus Psammogorgia comprises six valid species and two varieties, and three lectotypes and a new combination are proposed to establish the taxonomic status of these species.