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Abstract During two scientific expeditions between 2020 and 2022, direct surveys led to the discovery of free-living mesophotic foraminiferal-algal nodules along the coast of the NEOM region (northern Saudi Arabian Red Sea) where they form an unexpected benthic ecosystem in mesophotic water depths on the continental shelf. Being mostly spheroidal, the nodules are transported en masse down slope, into the deep water of the basin, where they stop accreting. Radiometric dating informs that these nodules can be more than two thousand years old and that they collectively contribute up to 66 g m−2 year−1 to the mesophotic benthic carbonate budget and account for at least 980 megatons of calcium carbonate, a substantial contribution considering the depauperate production of carbonate by other means in this light-limited environment. Our findings advance the knowledge of mesophotic biodiversity and carbonate production, and provide data that will inform conservation policies in the Saudi Arabian Red Sea.

Black corals (Hexacorallia: Antipatharia) are a major component of mesophotic and deep marine ecosystems. Due to their preference for light deprived environments, black corals have historically been considered azooxanthellate, yet recent works have found them in association with dinoflagellates of the family Symbiodiniaceae down to 396 m depth. While corals and Symbiodiniaceae generally establish a symbiotic relationship in shallow water environments, the implications of this association is less well understood at deeper depths, where low light penetration cannot sustain efficient photosynthetic activity for the algae. However, Symbiodinaceae are not obligate autotrophs, and their capacity for heterotrophic feeding categorizes them as mixotrophs. In this study, we investigated the presence and diversity of Symbiodiniaceae associated with the deep-sea black coral Bathypathes thermophila (Antipatharia: Schizopathidae), collected from 204 to 655 m depth in the Saudi Arabian Red Sea. Using high-throughput sequencing of the ITS2 region, we report (1) the deepest record to date of Symbiodiniaceae associated with an anthozoan from 655 m, and (2) the first Red Sea record of Antipatharia in association with Symbiodiniaceae. Our analyses revealed that 14 out of 27 colonies of B. thermophila were associated with Symbiodiniaceae of the genera Cladocopium and Durusdinium. We unveiled 16 novel ITS2 type profiles, possibly unique to black corals and/or to these depths, along with seven profiles that were already known from shallow-water hard corals. No significant pattern was detected in terms of community diversity in relation to depth or sampling locality. Our study supports the existence of black corals-Symbiodiniaceae association and warrants further research to better understand the evolutionary processes and physiological mechanisms driving this association, specifically in light deprived environments.

IntroductionThe Red Sea is a narrow rift basin characterized by latitudinal environmental gradients which shape the diversity and distribution of reef-dwelling organisms. Studies on Symbiodiniaceae associated with select hard coral taxa present species- specific assemblages and concordant variation patterns from the North to southeast Red Sea coast at depths shallower than 30 m. At mesophotic depths, however, algal diversity studies are rare. Here, we characterize for the first-time host-associated algal communities of a mesophotic specialist coral species, Leptoseris cf. striatus, along the Saudi Arabian Red Sea coast.MethodsWe sampled 56 coral colonies spanning the eastern Red Sea coastline from the Northern Red Sea to the Farasan Banks in the South, and across two sampling periods, Fall 2020 and Spring 2022. We used Next Generation Sequencing of the ITS2 marker region in conjunction with SymPortal to denote algal assemblages.Results and discussionOur results show a relatively stable coral species-specific interaction with algae from the genus Cladocopium along the examined latitudinal gradient, with the appearance, in a smaller proportion, of presumed thermally tolerant algal taxa in the genera Symbiodinium and Durusdinium during the warmer season (Fall 2020). Contrary to shallow water corals, our results do not show a change in Symbiodiniaceae community composition from North to South in this mesophotic specialist species. However, our study highlights for the first time that symbiont communities are subject to change over time at mesophotic depth, which could represent an important phenomenon to address in future studies.

Coral-dwelling gall crabs (Cryptochiridae) live in an obligate symbiosis with reef-building corals from shallow to deep waters. In particular, crabs of the genus Opecarcinus are known to occur across the tropical belt in association with the scleractinian family Agariciidae, down to a depth of 89 m. The Red Sea is a semi-enclosed basin that has long been recognized as a region of high marine biodiversity and endemism, with more than 230 decapod species recorded so far. There, nine Opecarcinus species are recorded from shallow and mesophotic corals. However, the occurrence of Opecarcinus below 30 m depth is documented only in the Saudi Arabian coast of the Northern Red Sea, and the rest of the Saudi Arabian Red Sea has remained unstudied. In this work, we assess the diversity and distribution of Opecarcinus from the mesophotic waters of the Saudi Arabian Red Sea. Through Remotely Operated Vehicles (ROV) and Submarines explorations, we collected 10 gall crab specimens associated with Agariciidae corals at mesophotic depths between 47 and 89 m. Two mitochondrial and one nuclear markers were used to obtain crab phylogenetic tree showing that three of the Opecarcinus species known from Red Sea shallow-water corals can also live at mesophotic depths. This is the first assessment of the depth distribution of the genus Opecarcinus in the Red Sea. It provides further evidence of the depth range adaptability of the Opecarcinus-Agariciidae association and highlights the need for a more in-depth investigation of the largely overlooked mesophotic coral-associated fauna.

IntroductionThe northern Red Sea has been coined a refuge for reef corals due to the exceptional thermal tolerance of these organisms. With ocean warming threatening coral reefs worldwide, a panoptic characterization of corals living in extreme conditions may provide insights into future responses of corals to environmental change. Among other factors, the genotype of the endosymbiotic algae in the family Symbiodiniaceae has been shown to have major implications on the distribution and resilience of their coral hosts. In this study, we aim at genotyping the Symbiodiniaceae communities associated with three depth generalist and one depth specialist coral species, characterized by the ability to withstand environmental conditions that are apparently limiting for other corals and occurring in a unique geographical region.MethodsWe sampled 50 corals from the northern Saudi Arabian Red Sea and the Gulf of Aqaba, covering a 97 m bathymetric gradient. We used high-throughput ITS2 gene sequencing and recovered different patterns of host–algal associations.Results and discussionThe majority of the recovered algal genotypes appeared host- and environment-specific, while others were more widely distributed. At large, coral specimens were overwhelmingly associated with symbionts from the genus Cladocopium and specifically with many previously undescribed genotypes. This suggests the selection of specific genotypes, which might confer resistance and/or resilience to their host counterparts. Interestingly, we found a limited association with Durusdinium spp. and other known tolerant taxa in mesophotic corals in the northern Red Sea, but not in the Gulf of Aqaba. The broad absence of Durusdinium spp., typically ascribed to be stress tolerant, warrants further investigation into Symbiodiniaceae species that convey environmental resilience. Our data will serve as a baseline to explore the occurrence of specific symbionts that might be contributing to coral acclimation and adaptation and to assay how biodiversity might be impacted if subjected to increasing stressors.

The diversity and evolution of the Red Sea invertebrates in mesophotic and deep-water benthic ecosystems remain largely unexplored. The Palaemonidae is a diversified family of caridean shrimps with numerous taxa in need of taxonomic revisions based on recent molecular analyses. The Red Sea mesophotic and bathyal palaemonid shrimps are largely unstudied. During recent expeditions off the Red Sea coast of Saudi Arabia, several palaemonid specimens were collected at a depth range of 88–494 m, spanning the mesophotic and bathyal zones. This material was examined morphologically and genetically to infer phylogenetic relationships among the Red Sea taxa and several other palaemonid genera. The concordant morphological and genetic data led to the description of two new genera and two new species. Moreover, one species was recorded in the Red Sea for the first time, with a new host record, whereas three further deep-water species, which do not occur in the Red Sea, were formally transferred to a different genus. As more exploration efforts are deployed, research on the diversity and evolutionary relationships among marine invertebrates from the Red Sea will further underline the uniqueness of its mesophotic and bathyal fauna.

Coral-dwelling gall crabs (Cryptochiridae) are obligate symbionts of stony corals and occur on shallow and deep reefs across the tropical belt. The circumtropical genus Opecarcinus associates with Agariciidae corals, a dominant component of Mesophotic Coral Ecosystems (MCEs). Here, we report the first Red Sea mesophotic record, with 89 m as the deepest record to date, for Opecarcinus—collected from Leptoseris cf mycetoseroides—from the NEOM marine area in Saudi Arabia. This observation reconfirms the depth range flexibility of Opecarcinus species and highlights the need for further mesophotic explorations of reef-associated fauna.