Mesophotic reef-building coral communities (∼30-120 m depth) remain largely unexplored, despite representing roughly three-quarters of the overall depth range at which tropical coral reef ecosystems occur. Although many coral species are restricted to shallow depths, several species occur across large depth ranges, including lower mesophotic depths. Yet, it remains unclear how such species can persist under extreme low-light conditions and how the different symbiotic partners associated with these corals contribute to facilitate such broad depth ranges. We assessed holobiont genetic diversity of the Caribbean coral Agaricia undata over depth in three localities of Colombia: San Andres Island (between 37 and 85 m), Cartagena (between 17 and 45 m) and "Parque Nacional Natural Corales de Profundidad" (between 77 and 87 m). We used a population genomics approach (NextRAD) for the coral host, and amplicon sequencing for the associated Symbiodinium (non-coding region of the plastid psbA minicircle) and prokaryotic (V4 region of the 16S rRNA gene) symbiont community. For the coral host, genetic structuring was only observed across geographic regions, but not between depths. Bayesian clustering and discriminant analysis of principal components revealed genetic structuring between the three regions, but not between shallow (<30 m), upper (≥30 and ≤60 m) and lower mesophotic (>60 m) depths. This pattern was confirmed when evaluating pairwise differentiation (F ST) between populations, with much higher values between regions (0.0467-0.1034) compared to between depths [within location; −0.0075-(−0.0007)]. Symbiotic partners, including seven types of zooxanthellae and 325 prokaryotic OTUs, did not exhibit partitioning across depths. All samples hosted Symbiodinium clade C3 and the type C3psbA_e was present in all depths. Alpha microbial diversity was not significantly different between zones (upper vs. lower), which community composition between coral colonies was similar in the two zones (ANOSIM, R = −0.079, P > 0.05). The coral microbiome was dominated by Uncultured Betaproteobacteria in the order EC94 (16%), Unknown-Bacteria (15%), family Gonzalez-Zapata et al. Mesophotic Holobiont Diversity Cenarchaeaceae (12 %), Burkholderiaceae (10%), and Hahellaceae (10%). The constant coral-holobiont composition along the studied depth range suggests that identity of the symbionts is not responsible for the coral's broad depth range and adaptation to low light environments.

Coral reef decline persists as a global issue with ties to climate change and human footprint. The SeaFlower Biosphere reserve includes some of the most isolated oceanic coral reefs in the Southwestern Caribbean, which provide natural experiments to test global and/or basin-wide factors affecting coral reefs. In this study, we compared coral and other substrate cover (algae, cyanobacteria, and octocorals), along population densities of keystone urchin species from two atolls (Serrana and Roncador Banks), during 1995, 2003, and 2015/2016. We also surveyed benthic foraminifera as a water quality proxy for coral growth in the last period. A steady reduction in coral cover was clearly observed at Roncador's lagoon, but not at Serrana's reefs, with significant differences between 1995 and 2015/2016. Percent cover of fleshy algae decreased significantly also at Roncador between 1995 and 2003 but did not change notably from 1995 to 2016 at Serrana. However, both Banks exhibited a loss in crustose coralline algae from 2003 to 2015/2016. Likewise, a reduction in bottom complexity, measured as bottom rugosity, was evident between 1995 and 2003. Roncador Bank had unprecedented high octocoral densities, which increased almost threefold from 2003 to 2015. In contrast, urchin densities were low in Roncador; only Diadema antillarum increased from 2003 to 2016 in Serrana Bank. The Foraminifera in Reef Assessment and Monitoring (FORAM) Index (FI) in the two Banks was below the range expected for healthy coral reefs. Although both Banks follow a reduction in CCA and CA cover, Roncador Bank also faces an alarming decline in coral cover, urchins and bottom complexity (rugosity) in contrast to increases in octocoral densities and potential loss of resilience and eutrophication suggested by the FI index. These unexpected findings led us to consider and discuss potential outcomes, where these reefs deteriorate (i.e., erode and drown) providing ideal conditions for octocoral growth. Hence, it is of utmost urgency to start monitoring reef budgets, octocorals and nutrient sources.

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