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Microbes are well-recognized members of the coral holobiont. However, little is known about the short-term dynamics of mucus-associated microbial communities under natural conditions and after disturbances, and how these dynamics relate to the host’s health. Here we examined the natural variability of prokaryotic communities (based on 16S ribosomal RNA gene amplicon sequencing) associating with the surface mucus layer (SML) of Porites astreoides, a species exhibiting cyclical mucus aging and shedding. Shifts in the prokaryotic community composition during mucus aging led to the prevalence of opportunistic and potentially pathogenic bacteria ( Verrucomicrobiaceae and Vibrionaceae ) in aged mucus and to a twofold increase in prokaryotic abundance. After the release of aged mucus sheets, the community reverted to its original state, dominated by Endozoicimonaceae and Oxalobacteraceae . Furthermore, we followed the fate of the coral holobiont upon depletion of its natural mucus microbiome through antibiotics treatment. After re-introduction to the reef, healthy-looking microbe-depleted corals started exhibiting clear signs of bleaching and necrosis. Recovery versus mortality of the P. astreoides holobiont was related to the degree of change in abundance distribution of the mucus microbiome. We conclude that the natural prokaryotic community inhabiting the coral SML contributes to coral health and that cyclical mucus shedding has a key role in coral microbiome dynamics.

Our rapidly warming climate is threatening coral reefs as thermal anomalies trigger mass coral bleaching events. Deep (or “mesophotic”) coral reefs are hypothesised to act as major ecological refuges from mass bleaching, but empirical assessments are limited. We evaluated the potential of mesophotic reefs within the Great Barrier Reef (GBR) and adjacent Coral Sea to act as thermal refuges by characterising long-term temperature conditions and assessing impacts during the 2016 mass bleaching event. We found that summer upwelling initially provided thermal relief at upper mesophotic depths (40 m), but then subsided resulting in anomalously warm temperatures even at depth. Bleaching impacts on the deep reefs were severe (40% bleached and 6% dead colonies at 40 m) but significantly lower than at shallower depths (60–69% bleached and 8–12% dead at 5-25 m). While we confirm that deep reefs can offer refuge from thermal stress, we highlight important caveats in terms of the transient nature of the protection and their limited ability to provide broad ecological refuge. It has been suggested that deep coral reefs offer a refuge against warming and mass bleaching. Here Frade et al. look at the 2016 bleaching event in the northern Great Barrier Reef and found that deep reefs initially acted as thermal refuges, though this effect lessened in the late summer months.

Background Coral reefs are facing unprecedented pressure on local and global scales. Sensitive and rapid markers for ecosystem stress are urgently needed to underpin effective management and restoration strategies. Although the fundamental contribution of microbes to the stability and functioning of coral reefs is widely recognised, it remains unclear how different reef microbiomes respond to environmental perturbations and whether microbiomes are sensitive enough to predict environmental anomalies that can lead to ecosystem stress. However, the lack of coral reef microbial baselines hinders our ability to study the link between shifts in microbiomes and ecosystem stress. In this study, we established a comprehensive microbial reference database for selected Great Barrier Reef sites to assess the diagnostic value of multiple free-living and host-associated reef microbiomes to infer the environmental state of coral reef ecosystems. Results A comprehensive microbial reference database, originating from multiple coral reef microbiomes (i.e. seawater, sediment, corals, sponges and macroalgae), was generated by 16S rRNA gene sequencing for 381 samples collected over the course of 16 months. By coupling this database to environmental parameters, we showed that the seawater microbiome has the greatest diagnostic value to infer shifts in the surrounding reef environment. In fact, 56% of the observed compositional variation in the microbiome was explained by environmental parameters, and temporal successions in the seawater microbiome were characterised by uniform community assembly patterns. Host-associated microbiomes, in contrast, were five-times less responsive to the environment and their community assembly patterns were generally less uniform. By applying a suite of indicator value and machine learning approaches, we further showed that seawater microbial community data provide an accurate prediction of temperature and eutrophication state (i.e. chlorophyll concentration and turbidity). Conclusion Our results reveal that free-living microbial communities have a high potential to infer environmental parameters due to their environmental sensitivity and predictability. This highlights the diagnostic value of microorganisms and illustrates how long-term coral reef monitoring initiatives could be enhanced by incorporating assessments of microbial communities in seawater. We therefore recommend timely integration of microbial sampling into current coral reef monitoring initiatives.

Species boundaries in scleractinian corals remain highly elusive due to conflicting patterns between morphological and molecular phylogenies, often caused by morphological plasticity, occurrence of cryptic species, incomplete lineage sorting or introgressive hybridization. Here, we use an integrated systematics approach, which combines reduced representation genome sequencing (nextRAD), micro-morphometric characterization, SEM analyses and compilation of life history traits, to infer phylogenetic relationships among closely related species in the Caribbean coral genus Madracis . In total, we analyzed 235 Madracis specimens from Curaçao and Bermuda collected from 10–90 m depth. Sequence- and SNP-based analyses for 115 samples generated unprecedented species resolution in Madracis , greatly supporting the morphology-based taxonomy of the current, accepted Caribbean species M. senaria , M. decactis , M. formosa , M. carmabi and M. mirabilis ( M. auretenra ). The exception was M. pharensis , in which we found evidence for three separate lineages, and for which we found signatures of admixture and introgression. These three M. pharensis lineages showed distinct depth distributions (thus classified as shallow, deep and very deep) and were partially distinguishable on the basis of fine microstructural elements of the collumella, septa and coenosteum. Further taxonomic comparisons are needed to formalize these putative cryptic species. Overall, our integrated systematics approach further resolves species relationships in the Caribbean genus Madracis , supports the morphological descriptions for most of the recognized species, but also reveals the existence of cryptic diversity in groups marked by high admixture, thus suggesting hybridization as a driving force in coral species diversity.

The composition, ecology and environmental conditions of mesophotic coral ecosystems near the lower limits of their bathymetric distributions remain poorly understood. Here we provide the first in-depth assessment of a lower mesophotic coral community (60–100 m) in the Southern Caribbean through visual submersible surveys, genotyping of coral host-endosymbiont assemblages, temperature monitoring and a growth experiment. The lower mesophotic zone harbored a specialized coral community consisting of predominantly Agaricia grahamae , Agaricia undata and a “deep-water” lineage of Madracis pharensis , with large colonies of these species observed close to their lower distribution limit of ~90 m depth. All three species associated with “deep-specialist” photosynthetic endosymbionts ( Symbiodinium ). Fragments of A. grahamae exhibited growth rates at 60 m similar to those observed for shallow Agaricia colonies (~2–3 cm yr −1 ), but showed bleaching and (partial) mortality when transplanted to 100 m. We propose that the strong reduction of temperature over depth (Δ5°C from 40 to 100 m depth) may play an important contributing role in determining lower depth limits of mesophotic coral communities in this region. Rather than a marginal extension of the reef slope, the lower mesophotic represents a specialized community and as such warrants specific consideration from science and management.

Corals are associated with diverse microbial assemblages; however, the spatial-temporal dynamics of intra-species microbial interactions are poorly understood. The coral-associated microbial community varies substantially between tissue and mucus microhabitats; however, the factors controlling the occurrence, abundance, and distribution of microbial taxa over time have rarely been explored for different coral compartments simultaneously. Here, we test (1) differentiation in microbiome diversity and composition between coral compartments (surface mucus and tissue) of two Acropora hosts ( A. tenuis and A. millepora ) common along inshore reefs of the Great Barrier Reef, as well as (2) the potential linkage between shifts in individual coral microbiome families and underlying host and environmental parameters. Amplicon based 16S ribosomal RNA gene sequencing of 136 samples collected over 14 months, revealed significant differences in bacterial richness, diversity and community structure among mucus, tissue and the surrounding seawater. Seawater samples were dominated by members of the Synechococcaceae and Pelagibacteraceae bacterial families. The mucus microbiome of Acropora spp. was dominated by members of Flavobacteriaceae, Synechococcaceae and Rhodobacteraceae and the tissue was dominated by Endozoicimonaceae. Mucus microbiome in both Acropora species was primarily correlated with seawater parameters including levels of chlorophyll a, ammonium, particulate organic carbon and the sum of nitrate and nitrite. In contrast, the correlation of the tissue microbiome to the measured environmental (i.e., seawater parameters) and host health physiological factors differed between host species, suggesting host-specific modulation of the tissue-associated microbiome to intrinsic and extrinsic factors. Furthermore, the correlation between individual coral microbiome members and environmental factors provides novel insights into coral microbiome-by-environment dynamics and hence has potential implications for current reef restoration and management efforts (e.g. microbial monitoring and observatory programs).

Comparative studies on the distribution of archaeal versus bacterial communities associated with the surface mucus layer of corals have rarely taken place. It has therefore remained enigmatic whether mucus-associated archaeal and bacterial communities exhibit a similar specificity towards coral hosts and whether they vary in the same fashion over spatial gradients and between reef locations. We used microbial community profiling (terminal-restriction fragment length polymorphism, T-RFLP) and clone library sequencing of the 16S rRNA gene to compare the diversity and community structure of dominant archaeal and bacterial communities associating with the mucus of three common reef-building coral species (Porites astreoides, Siderastrea siderea and Orbicella annularis) over different spatial scales on a Caribbean fringing reef. Sampling locations included three reef sites, three reef patches within each site and two depths. Reference sediment samples and ambient water were also taken for each of the 18 sampling locations resulting in a total of 239 samples. While only 41% of the bacterial operational taxonomic units (OTUs) characterized by T-RFLP were shared between mucus and the ambient water or sediment, for archaeal OTUs this percentage was 2-fold higher (78%). About half of the mucus-associated OTUs (44% and 58% of bacterial and archaeal OTUs, respectively) were shared between the three coral species. Our multivariate statistical analysis (ANOSIM, PERMANOVA and CCA) showed that while the bacterial community composition was determined by habitat (mucus, sediment or seawater), host coral species, location and spatial distance, the archaeal community composition was solely determined by the habitat. This study highlights that mucus-associated archaeal and bacterial communities differ in their degree of community turnover over reefs and in their host-specificity.

Coral reefs are increasingly threatened by heat stress events leading to coral bleaching. In 2016, a mass bleaching event affected large parts of the Great Barrier Reef (GBR). Whilst bleaching severity and coral mortality are usually monitored throughout major bleaching events, other health indicators, such as changes in microbial partners, are rarely assessed. We examined the impact of the 2016 bleaching event on the composition of the microbial communities in the coral Pocillopora acuta at Havannah Island Pandora reef, separated by 12 km on the inshore central GBR. Corals experienced moderate heat stress (3.6 and 5.3 degree heating weeks), inducing major bleaching (30–60%) at the coral community level. Samples were partitioned according to Symbiodiniaceae densities into three bleaching severity categories (mild, moderate, and severe). Whilst Symbiodiniaceae densities were similar at both reef locations, sequencing of the Symbiodiniaceae ITS2 and prokaryotic 16S rRNA genes revealed that microbial communities were significantly different between reefs, but not according to bleaching severity. Symbiodiniaceae composition was dominated by the genus Cladocopium with low abundances of Durusdinium detected in moderately and severely bleached colonies at both sites, despite site-specific ITS2 profiles. Bacterial communities were dominated by Proteobacteria and were almost entirely lacking the common Pocilloporid associate Endozoicomonas regardless of bleaching severity. Strikingly, only 11.2% of the bacterial Amplicon Sequencing Variants (ASVs) were shared between sites. This reef specificity was driven by 165 ASVs, mainly from the family Rhodobacteraceae. Comparison with previous studies suggests that the moderate heat stress experienced on the central GBR in 2016 caused the near-complete absence of Endozoicomonas. Symbiodiniaceae and bacteria (particularly Rhodobacteraceae) can be vertically transmitted in P. acuta, and larval propagation can be spatially restricted for this brooding species. Our results demonstrate that, unlike bleaching severity, location-specific factors and species-specific life history traits might have been paramount in shaping the P. acuta microbiome.

Museum collections are an important source for resolving taxonomic issues and species delimitation. Type specimens as name-bearing specimens, traditionally used in morphology-based taxonomy, are, due to the progress in historical DNA methodology, increasingly used in molecular taxonomic studies. Museum collections are subject to constant deterioration and major disasters. The digitisation of collections offers a partial solution to these problems and makes museum collections more accessible to the wider scientific community. The Extended Specimen Approach (ESA) is a method of digitisation that goes beyond the physical specimen to include the historical information stored in the collection. The collections of the Natural History Museum Vienna represent one of the largest non-university research centres in Europe and, due to their size and numerous type specimens, are frequently used for taxonomic studies by visiting and resident scientists. Recently, a version of ESA was presented in the common catalogue of the Fish and Evertebrata Varia collections and extended to include genetic information on type specimens in a case study of a torpedo ray. Here the case study was extended to a heterogeneous selection of historical type series from different collections with the type locality of Vienna. The goal was to apply the ESA, including genetic data on a selected set of type material: three parasitic worms, three myriapods, two insects, twelve fishes, and one bird species. Five hundred digital items (photographs, X-rays, scans) were produced, and genetic analysis was successful in eleven of the 21 type series. In one case a complete mitochondrial genome was assembled, and in another case ten short fragments (100–230 bp) of the cytochrome oxidase I gene were amplified and sequenced. For five type series, genetic analysis confirmed their taxonomic status as previously recognised synonyms, and for one the analysis supported its status as a distinct species. For two species, genetic information was provided for the first time. This catalogue thus demonstrates the usefulness of ESA in providing digitised data of types that can be easily made available to scientists worldwide for further study.