Trade-off in a reef-building coral after six years of thermal acclimation.

There is growing evidence that reef-building corals can acclimate to novel and challenging thermal conditions. However, potential trade-offs that accompany acclimation remain largely unexplored. We investigated physiological trade-offs in colonies of a globally abundant coral species (Pocillopora acuta) that were acclimated ex situ to an elevated temperature of 31 °C (i.e., 1 °C above their bleaching threshold) for six years. By comparing them to conspecifics maintained at a cooler temperature, we found that the energy storage of corals was prioritized over skeletal growth at the elevated temperature. This was associated with the formation of higher density skeletons, lower calcification rates and consequently lower skeletal extension rates, which entails ramifications for future reef-building processes, structural complexity and reef community composition. Furthermore, symbionts were physiologically compromised at 31 °C and had overall lower energy reserves, likely due to greater exploitation by their host, resulting in an overall lower stress resilience of the holobiont. Our study shows how biological trade-offs of thermal acclimation unfold, helping to refine our picture of future coral reef trajectories. Importantly, our observations in this six-year study do not align with observations of short-term studies, where elevated temperatures were often associated with the depletion of energy reserves, highlighting the importance of studying acclimation of organisms at relevant biological scales.

Horizon scanning the application of probiotics for wildlife.

The provision of probiotics benefits the health of a wide range of organisms, from humans to animals and plants. Probiotics can enhance stress resilience of endangered organisms, many of which are critically threatened by anthropogenic impacts. The use of so-called 'probiotics for wildlife' is a nascent application, and the field needs to reflect on standards for its development, testing, validation, risk assessment, and deployment. Here, we identify the main challenges of this emerging intervention and provide a roadmap to validate the effectiveness of wildlife probiotics. We cover the essential use of inert negative controls in trials and the investigation of the probiotic mechanisms of action. We also suggest alternative microbial therapies that could be tested in parallel with the probiotic application. Our recommendations align approaches used for humans, aquaculture, and plants to the emerging concept and use of probiotics for wildlife.

Harnessing the microbiome to prevent global biodiversity loss.

Global biodiversity loss and mass extinction of species are two of the most critical environmental issues the world is currently facing, resulting in the disruption of various ecosystems central to environmental functions and human health. Microbiome-targeted interventions, such as probiotics and microbiome transplants, are emerging as potential options to reverse deterioration of biodiversity and increase the resilience of wildlife and ecosystems. However, the implementation of these interventions is urgently needed. We summarize the current concepts, bottlenecks and ethical aspects encompassing the careful and responsible management of ecosystem resources using the microbiome (termed microbiome stewardship) to rehabilitate organisms and ecosystem functions. We propose a real-world application framework to guide environmental and wildlife probiotic applications. This framework details steps that must be taken in the upscaling process while weighing risks against the high toll of inaction. In doing so, we draw parallels with other aspects of contemporary science moving swiftly in the face of urgent global challenges.

A roadmap to understanding diversity and function of coral reef-associated fungi.

Tropical coral reefs are hotspots of marine productivity, owing to the association of reef-building corals with endosymbiotic algae and metabolically diverse bacterial communities. However, the functional importance of fungi, well-known for their contribution to shaping terrestrial ecosystems and global nutrient cycles, remains underexplored on coral reefs. We here conceptualize how fungal functional traits may have facilitated the spread, diversification, and ecological adaptation of marine fungi on coral reefs. We propose that functions of reef-associated fungi may be diverse and go beyond their hitherto described roles of pathogens and bioeroders, including but not limited to reef-scale biogeochemical cycles and the structuring of coral-associated and environmental microbiomes via chemical mediation. Recent technological and conceptual advances will allow the elucidation of the physiological, ecological, and chemical contributions of understudied marine fungi to coral holobiont and reef ecosystem functioning and health and may help provide an outlook for reef management actions.

Towards enhancing coral heat tolerance: a "microbiome transplantation" treatment using inoculations of homogenized coral tissues.

BACKGROUND: Microbiome manipulation could enhance heat tolerance and help corals survive the pressures of ocean warming. We conducted coral microbiome transplantation (CMT) experiments using the reef-building corals, Pocillopora and Porites, and investigated whether this technique can benefit coral heat resistance while modifying the bacterial microbiome. Initially, heat-tolerant donors were identified in the wild. We then used fresh homogenates made from coral donor tissues to inoculate conspecific, heat-susceptible recipients and documented their bleaching responses and microbiomes by 16S rRNA gene metabarcoding. RESULTS: Recipients of both coral species bleached at lower rates compared to the control group when exposed to short-term heat stress (34 °C). One hundred twelve (Pocillopora sp.) and sixteen (Porites sp.) donor-specific bacterial species were identified in the microbiomes of recipients indicating transmission of bacteria. The amplicon sequence variants of the majority of these transmitted bacteria belonged to known, putatively symbiotic bacterial taxa of corals and were linked to the observed beneficial effect on the coral stress response. Microbiome dynamics in our experiments support the notion that microbiome community evenness and dominance of one or few bacterial species, rather than host-species identity, were drivers for microbiome stability in a holobiont context. CONCLUSIONS: Our results suggest that coral recipients likely favor the uptake of putative bacterial symbionts, recommending to include these taxonomic groups in future coral probiotics screening efforts. Our study suggests a scenario where these donor-specific bacterial symbionts might have been more efficient in supporting the recipients to resist heat stress compared to the native symbionts present in the control group. These findings urgently call for further experimental investigation of the mechanisms of action underlying the beneficial effect of CMT and for field-based long-term studies testing the persistence of the effect. Video abstract.

The Native Microbiome is Crucial for Offspring Generation and Fitness of Aurelia aurita.

All multicellular organisms are associated with microbial communities, ultimately forming a metaorganism. Several studies conducted on well-established model organisms point to immunological, metabolic, and behavioral benefits of the associated microbiota for the host. Consequently, a microbiome can influence the physiology of a host; moreover, microbial community shifts can affect host health and fitness. The present study aimed to evaluate the significance and functional role of the native microbiota for life cycle transitions and fitness of the cnidarian moon jellyfish Aurelia aurita A comprehensive host fitness experiment was conducted studying the polyp life stage and integrating 12 combinations of treatments with microbiota modification (sterile conditions, foreign food bacteria, and potential pathogens). Asexual reproduction, e.g., generation of daughter polyps, and the formation and release of ephyrae were highly affected in the absence of the native microbiota, ultimately resulting in a halt of strobilation and ephyra release. Assessment of further fitness traits showed that health, growth, and feeding rate were decreased in the absence and upon community changes of the native microbiota, e.g., when challenged with selected bacteria. Moreover, changes in microbial community patterns were detected by 16S rRNA amplicon sequencing during the course of the experiment. This demonstrated that six operational taxonomic units (OTUs) significantly correlated and explained up to 97% of fitness data variability, strongly supporting the association of impaired fitness with the absence/presence of specific bacteria. Conclusively, our study provides new insights into the importance and function of the microbiome for asexual reproduction, health, and fitness of the basal metazoan A. auritaIMPORTANCE All multicellular organisms are associated with a diverse and specific community of microorganisms; consequently, the microbiome is of fundamental importance for health and fitness of the multicellular host. However, studies on microbiome contribution to host fitness are in their infancy, in particular, for less well-established hosts such as the moon jellyfish Aurelia aurita Here, we studied the impact of the native microbiome on the asexual reproduction and on further fitness traits (health, growth, and feeding) of the basal metazoan due to induced changes in its microbiome. We observed significant impact on all fitness traits analyzed, in particular, in the absence of the protective microbial shield and when challenged with marine potentially pathogenic bacterial isolates. Notable is the identified crucial importance of the native microbiome for the generation of offspring, consequently affecting life cycle decisions. Thus, we conclude that the microbiome is essential for the maintenance of a healthy metaorganism.

In situ observations of coral bleaching in the central Saudi Arabian Red Sea during the 2015/2016 global coral bleaching event.

Coral bleaching continues to be one of the most devastating and immediate impacts of climate change on coral reef ecosystems worldwide. In 2015, a major bleaching event was declared as the "3rd global coral bleaching event" by the United States National Oceanic and Atmospheric Administration, impacting a large number of reefs in every major ocean. The Red Sea was no exception, and we present herein in situ observations of the status of coral reefs in the central Saudi Arabian Red Sea from September 2015, following extended periods of high temperatures reaching upwards of 32.5°C in our study area. We examined eleven reefs using line-intercept transects at three different depths, including all reefs that were surveyed during a previous bleaching event in 2010. Bleaching was most prevalent on inshore reefs (55.6% ± 14.6% of live coral cover exhibited bleaching) and on shallower transects (41% ± 10.2% of live corals surveyed at 5m depth) within reefs. Similar taxonomic groups (e.g., Agariciidae) were affected in 2015 and in 2010. Most interestingly, Acropora and Porites had similar bleaching rates (~30% each) and similar relative coral cover (~7% each) across all reefs in 2015. Coral genera with the highest levels of bleaching (>60%) were also among the rarest (<1% of coral cover) in 2015. While this bodes well for the relative retention of coral cover, it may ultimately lead to decreased species richness, often considered an important component of a healthy coral reef. The resultant long-term changes in these coral reef communities remain to be seen.

Transcriptomes and expression profiling of deep-sea corals from the Red Sea provide insight into the biology of azooxanthellate corals.

Despite the importance of deep-sea corals, our current understanding of their ecology and evolution is limited due to difficulties in sampling and studying deep-sea environments. Moreover, a recent re-evaluation of habitat limitations has been suggested after characterization of deep-sea corals in the Red Sea, where they live at temperatures of above 20 °C at low oxygen concentrations. To gain further insight into the biology of deep-sea corals, we produced reference transcriptomes and studied gene expression of three deep-sea coral species from the Red Sea, i.e. Dendrophyllia sp., Eguchipsammia fistula, and Rhizotrochus typus. Our analyses suggest that deep-sea coral employ mitochondrial hypometabolism and anaerobic glycolysis to manage low oxygen conditions present in the Red Sea. Notably, we found expression of genes related to surface cilia motion that presumably enhance small particle transport rates in the oligotrophic deep-sea environment. This is the first study to characterize transcriptomes and in situ gene expression for deep-sea corals. Our work offers several mechanisms by which deep-sea corals might cope with the distinct environmental conditions present in the Red Sea As such, our data provide direction for future research and further insight to organismal response of deep-sea coral to environmental change and ocean warming.

Microbial community composition of deep-sea corals from the Red Sea provides insight into functional adaption to a unique environment.

Microbes associated with deep-sea corals remain poorly studied. The lack of symbiotic algae suggests that associated microbes may play a fundamental role in maintaining a viable coral host via acquisition and recycling of nutrients. Here we employed 16 S rRNA gene sequencing to study bacterial communities of three deep-sea scleractinian corals from the Red Sea, Dendrophyllia sp., Eguchipsammia fistula, and Rhizotrochus typus. We found diverse, species-specific microbiomes, distinct from the surrounding seawater. Microbiomes were comprised of few abundant bacteria, which constituted the majority of sequences (up to 58% depending on the coral species). In addition, we found a high diversity of rare bacteria (taxa at <1% abundance comprised >90% of all bacteria). Interestingly, we identified anaerobic bacteria, potentially providing metabolic functions at low oxygen conditions, as well as bacteria harboring the potential to degrade crude oil components. Considering the presence of oil and gas fields in the Red Sea, these bacteria may unlock this carbon source for the coral host. In conclusion, the prevailing environmental conditions of the deep Red Sea (>20 °C, <2 mg oxygen L-1) may require distinct functional adaptations, and our data suggest that bacterial communities may contribute to coral functioning in this challenging environment.

Year-Long Monitoring of Physico-Chemical and Biological Variables Provide a Comparative Baseline of Coral Reef Functioning in the Central Red Sea.

Coral reefs in the central Red Sea are sparsely studied and in situ data on physico-chemical and key biotic variables that provide an important comparative baseline are missing. To address this gap, we simultaneously monitored three reefs along a cross-shelf gradient for an entire year over four seasons, collecting data on currents, temperature, salinity, dissolved oxygen (DO), chlorophyll-a, turbidity, inorganic nutrients, sedimentation, bacterial communities of reef water, and bacterial and algal composition of epilithic biofilms. Summer temperature (29-33°C) and salinity (39 PSU) exceeded average global maxima for coral reefs, whereas DO concentration was low (2-4 mg L-1). While temperature and salinity differences were most pronounced between seasons, DO, chlorophyll-a, turbidity, and sedimentation varied most between reefs. Similarly, biotic communities were highly dynamic between reefs and seasons. Differences in bacterial biofilms were driven by four abundant families: Rhodobacteraceae, Flavobacteriaceae, Flammeovirgaceae, and Pseudanabaenaceae. In algal biofilms, green crusts, brown crusts, and crustose coralline algae were most abundant and accounted for most of the variability of the communities. Higher bacterial diversity of biofilms coincided with increased algal cover during spring and summer. By employing multivariate matching, we identified temperature, salinity, DO, and chlorophyll-a as the main contributing physico-chemical drivers of biotic community structures. These parameters are forecast to change most with the progression of ocean warming and increased nutrient input, which suggests an effect on the recruitment of Red Sea benthic communities as a result of climate change and anthropogenic influence. In conclusion, our study provides insight into coral reef functioning in the Red Sea and a comparative baseline to support coral reef studies in the region.

Long-term salinity tolerance is accompanied by major restructuring of the coral bacterial microbiome.

Scleractinian corals are assumed to be stenohaline osmoconformers, although they are frequently subjected to variations in seawater salinity due to precipitation, freshwater run-off and other processes. Observed responses to altered salinity levels include differences in photosynthetic performance, respiration and increased bleaching and mortality of the coral host and its algal symbiont, but a study looking at bacterial community changes is lacking. Here, we exposed the coral Fungia granulosa to strongly increased salinity levels in short- and long-term experiments to disentangle temporal and compartment effects of the coral holobiont (i.e. coral host, symbiotic algae and associated bacteria). Our results show a significant reduction in calcification and photosynthesis, but a stable microbiome after short-term exposure to high-salinity levels. By comparison, long-term exposure yielded unchanged photosynthesis levels and visually healthy coral colonies indicating long-term acclimation to high-salinity levels that were accompanied by a major coral microbiome restructuring. Importantly, a bacterium in the family Rhodobacteraceae was succeeded by Pseudomonas veronii as the numerically most abundant taxon. Further, taxonomy-based functional profiling indicates a shift in the bacterial community towards increased osmolyte production, sulphur oxidation and nitrogen fixation. Our study highlights that bacterial community composition in corals can change within days to weeks under altered environmental conditions, where shifts in the microbiome may enable adjustment of the coral to a more advantageous holobiont composition.

Coral microbial community dynamics in response to anthropogenic impacts near a major city in the central Red Sea.

Coral-associated bacteria play an increasingly recognized part in coral health. We investigated the effect of local anthropogenic impacts on coral microbial communities on reefs near Jeddah, the largest city on the Saudi Arabian coast of the central Red Sea. We analyzed the bacterial community structure of water and corals (Pocillopora verrucosa and Acropora hemprichii) at sites that were relatively unimpacted, exposed to sedimentation & local sewage, or in the discharge area of municipal wastewaters. Coral microbial communities were significantly different at impacted sites: in both corals the main symbiotic taxon decreased in abundance. In contrast, opportunistic bacterial families, such as e.g. Vibrionaceae and Rhodobacteraceae, were more abundant in corals at impacted sites. In conclusion, microbial community response revealed a measurable footprint of anthropogenic impacts to coral ecosystems close to Jeddah, even though the corals appeared visually healthy.

Captive rearing of the deep-sea coral Eguchipsammia fistula from the Red Sea demonstrates remarkable physiological plasticity.

The presence of the cosmopolitan deep-sea coral Eguchipsammia fistula has recently been documented in the Red Sea, occurring in warm (>20 °C), oxygen- and nutrient-limited habitats. We collected colonies of this species from the central Red Sea that successfully resided in aquaria for more than one year. During this period the corals were exposed to increased oxygen levels and nutrition ad libitum unlike in their natural habitat. Specimens of long-term reared E. fistula colonies were incubated for 24 h and calcification (G) as well as respiration rates (R) were measured. In comparison to on-board measurements of G and R rates on freshly collected specimens, we found that G was increased while R was decreased. E. fistula shows extensive tissue growth and polyp proliferation in aquaculture and can be kept at conditions that notably differ from its natural habitat. Its ability to cope with rapid and prolonged changes in regard to prevailing environmental conditions indicates a wide physiological plasticity. This may explain in part the cosmopolitan distribution of this species and emphasizes its value as a deep-sea coral model to study mechanisms of acclimation and adaptation.