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

      Roik, Anna; Röthig, Till; Roder, Cornelia; Müller, Paul J.; Voolstra, Christian R.; King Abdullah University of Science and Technology (KAUST); Red Sea Research Center, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia; Red Sea Research Center, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia; Red Sea Research Center, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia; Coastal and Marine Resources Core Lab, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia; et al. (2015-01-20)
      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.
    • Coral reef carbonate budgets and ecological drivers in the central Red Sea: a naturally high temperature and high total alkalinity environment.

      Roik, Anna; Röthig, Till; Pogoreutz, Claudia; Saderne, Vincent; Voolstra, Christian R.; King Abdullah University of Science and Technology (KAUST); University of Derby (European Geosciences Union, 2018-10-26)
      The structural framework provided by corals is crucial for reef ecosystem function and services, but high seawater temperatures can be detrimental to the calcification capacity of reef-building organisms. The Red Sea is very warm, but total alkalinity (TA) is naturally high and beneficial for reef accretion. To date, we know little about how such detrimental and beneficial abiotic factors affect each other and the balance between calcification and erosion on Red Sea coral reefs, i.e., overall reef growth, in this unique ocean basin. To provide estimates of present-day reef growth dynamics in the central Red Sea, we measured two metrics of reef growth, i.e., in situ net-accretion/-erosion rates (Gnet) determined by deployment of limestone blocks and ecosystem-scale carbonate budgets (Gbudget), along a crossshelf gradient (25 km, encompassing nearshore, midshore, and offshore reefs). Along this gradient, we assessed multiple abiotic (i.e., temperature, salinity, diurnal pH fluctuation, inorganic nutrients, and TA) and biotic (i.e., calcifier and epilithic bioeroder communities) variables. Both reef growth metrics revealed similar patterns from nearshore to offshore: net-erosive, neutral, and net-accretion states. The average cross-shelf Gbudget was 0.66 kg CaCO3 m−2 yr−1 , with the highest budget of 2.44 kg CaCO3 m−2 yr−1 measured in the offshore reef. These data are comparable to the contemporary Gbudgets from the western Atlantic and Indian oceans, but lie well below “optimal reef production” (5–10 kg CaCO3 m−2 yr−1 ) and below maxima recently recorded in remote high coral cover reef sites. However, the erosive forces observed in the Red Sea nearshore reef contributed less than observed elsewhere. A higher TA accompanied reef growth across the shelf gradient, whereas stronger diurnal pH fluctuations were associated with negative carbonate budgets. Noteworthy for this oligotrophic region was the positive effect of phosphate, which is a central micronutrient for reef building corals. While parrotfish contributed substantially to bioerosion, our dataset also highlights coralline algae as important local reef builders. Altogether, our study establishes a baseline for reef growth in the central Red Sea that should be useful in assessing trajectories of reef growth capacity under current and future ocean scenarios
    • Distinct bacterial microbiomes associate with the deep-sea coral Eguchipsammia fistula from the Red Sea and from aquaria settings.

      Röthig, Till; Roik, Anna; Yum, Lauren K.; Voolstra, Christian R.; King Abdullah University of Science and Technology (KAUST) (Frontiers Media, 2017-08-10)
      Microbial communities associated with deep-sea corals are beginning to be studied in earnest and the contribution of the microbiome to host organismal function remains to be investigated. In this regard, the ability of the microbiome to adjust to prevailing environmental conditions might provide clues to its functional importance. In this study, we characterized bacterial community composition associated with the deep-sea coral Eguchipsammia fistula under natural (in situ) and aquaria (ex situ) settings using 16S rRNA gene amplicon sequencing. We compared freshly collected Red Sea coral specimens with those reared for >1 year at conditions that partially differed from the natural environment, in particular regarding increased oxygen and food availability under ex situ conditions. We found substantial differences between the microbiomes associated with corals under both environmental settings. The core microbiome comprised only six bacterial taxa consistently present in all corals, whereas the majority of bacteria were exclusively associated either with freshly collected corals or corals under long-term reared aquaria settings. Putative functional profiling of microbial communities showed that corals in their natural habitat were enriched for processes indicative of a carbon- and nitrogen-limited environment, which might be reflective of differences in diet under in situ and ex situ conditions. The ability of E. fistula to harbor distinct microbiomes under different environmental settings might contribute to the flexibility and phenotypic plasticity of this cosmopolitan coral. Future efforts should further assess the role of these different bacteria in holobiont function, in particular since E. fistula is naturally present in markedly different environments.
    • High salinity tolerance of the Red Sea coral Fungia granulosa under desalination concentrate discharge conditions: an in situ photophysiology experiment.

      van der Merwe, Riaan; Röthig, Till; Voolstra, Christian R.; Ochsenkühn, Michael A.; Lattemann, Sabine; Amy, Gary L.; King Abdullah University of Science and Technology (KAUST) (Frontiers, 2014-11-10)
      Seawater reverse osmosis desalination concentrate may have chronic and/or acute impacts on the marine ecosystems in the near-field area of the discharge. Environmental impact of the desalination plant discharge is supposedly site- and volumetric- specific, and also depends on the salinity tolerance of the organisms inhabiting the water column in and around a discharge environment. Scientific studies that aim to understand possible impacts of elevated salinity levels are important to assess detrimental effects to organisms, especially for species with no mechanism of osmoregulation, e.g., presumably corals. Previous studies on corals indicate sensitivity toward hypo- and hyper-saline environments with small changes in salinity already affecting coral physiology. In order to evaluate sensitivity of Red Sea corals to increased salinity levels, we conducted a long-term (29 days) in situ salinity tolerance transect study at an offshore seawater reverse osmosis (SWRO) discharge on the coral Fungia granulosa. While we measured a pronounced increase in salinity and temperature at the direct outlet of the discharge structure, effects were indistinguishable from the surrounding environment at a distance of 5 m. Interestingly, corals were not affected by varying salinity levels as indicated by measurements of the photosynthetic efficiency. Similarly, cultured coral symbionts of the genus Symbiodinium displayed remarkable tolerance levels in regard to hypo- and hypersaline treatments. Our data suggest that increased salinity and temperature levels from discharge outlets wear off quickly in the surrounding environment. Furthermore, F. granulosa seem to tolerate levels of salinity that are distinctively higher than reported for other corals previously. It remains to be determined whether Red Sea corals in general display increased salinity tolerance, and whether this is related to prevailing levels of high(er) salinity in the Red Sea in comparison to other oceans.
    • In situ observations of coral bleaching in the central Saudi Arabian Red Sea during the 2015/2016 global coral bleaching event.

      Monroe, Alison A.; Ziegler, Maren; Roik, Anna; Röthig, Till; Hardenstine, Royale S.; Emms, Madeleine A.; Jensen, Thor; Voolstra, Christian R.; Berumen, Michael L.; King Abdullah University of Science and Technology (KAUST); et al. (PLOS ONE, 2018-04-19)
      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.
    • Long-term salinity tolerance is accompanied by major restructuring of the coral bacterial microbiome.

      Röthig, Till; Ochsenkühn, Michael A.; Roik, Anna; van der Merwe, Riaan; Voolstra, Christian R.; King Abdullah University of Science and Technology (KAUST); Red Sea Research Center; King Abdullah University of Science and Technology (KAUST); Thuwal 23955-6900 Saudi Arabia; Biological and Organometallic Catalysis Laboratories; King Abdullah University of Science and Technology (KAUST); Thuwal 23955-6900 Saudi Arabia; Red Sea Research Center; King Abdullah University of Science and Technology (KAUST); Thuwal 23955-6900 Saudi Arabia; Red Sea Research Center; King Abdullah University of Science and Technology (KAUST); Thuwal 23955-6900 Saudi Arabia; et al. (Wiley., 2016-02-03)
      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.
    • Microbial community composition of deep-sea corals from the Red Sea provides insight into functional adaption to a unique environment

      Röthig, Till; Yum, Lauren K.; Kremb, Stephan G.; Roik, Anna; Voolstra, Christian R.; King Abdullah University of Science and Technology (KAUST) (Nature Research, 2017-03-17)
      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.
    • Repeated observations of cetaceans and carcharhiniformes associations in the Red Sea

      Röthig, Till; Spaet, Julia L. Y.; Kattan, Alexander; Schulz, Isabelle K.; Roberts, May; Roik, Anna; Voolstra, Christian R.; King Abdullah University of Science and Technology (KAUST) (Springer, 2015-06-27)
    • The role of floridoside in osmoadaptation of coral-associated algal endosymbionts to high-salinity conditions.

      Ochsenkühn, Michael A.; Röthig, Till; D’Angelo, Cecilia; Wiedenmann, Jörg; Voolstra, Christian R.; King Abdullah University of Science and Technology (KAUST); University of Southampton; New York University Abu Dhabi (American Association for the Advancement of Science, 2017-08-16)
      The endosymbiosis between Symbiodinium dinoflagellates and stony corals provides the foundation of coral reef ecosystems. The survival of these ecosystems is under threat at a global scale, and better knowledge is needed to conceive strategies for mitigating future reef loss. Environmental disturbance imposing temperature, salinity, and nutrient stress can lead to the loss of the Symbiodinium partner, causing so-called coral bleaching. Some of the most thermotolerant coral-Symbiodinium associations occur in the Persian/Arabian Gulf and the Red Sea, which also represent the most saline coral habitats. We studied whether Symbiodinium alter their metabolite content in response to high-salinity environments. We found that Symbiodinium cells exposed to high salinity produced high levels of the osmolyte 2-O-glycerol-α-d-galactopyranoside (floridoside), both in vitro and in their coral host animals, thereby increasing their capacity and, putatively, the capacity of the holobiont to cope with the effects of osmotic stress in extreme environments. Given that floridoside has been previously shown to also act as an antioxidant, this osmolyte may serve a dual function: first, to serve as a compatible organic osmolyte accumulated by Symbiodinium in response to elevated salinities and, second, to counter reactive oxygen species produced as a consequence of potential salinity and heat stress.
    • Spatial and seasonal reef calcification in corals and calcareous crusts in the central Red Sea.

      Roik, Anna; Roder, Cornelia; Röthig, Till; Voolstra, Christian R.; King Abdullah University of Science and Technology (KAUST) (Springer., 2015-12-14)
      The existence of coral reef ecosystems critically relies on the reef carbonate framework produced by scleractinian corals and calcareous crusts (i.e., crustose coralline algae). While the Red Sea harbors one of the longest connected reef systems in the world, detailed calcification data are only available from the northernmost part. To fill this knowledge gap, we measured in situ calcification rates of primary and secondary reef builders in the central Red Sea. We collected data on the major habitat-forming coral genera Porites, Acropora, and Pocillopora and also on calcareous crusts (CC) in a spatioseasonal framework. The scope of the study comprised sheltered and exposed sites of three reefs along a crossshelf gradient and over four seasons of the year. Calcification of all coral genera was consistent across the shelf and highest in spring. In addition, Pocillopora showed increased calcification at exposed reef sites. In contrast, CC calcification increased from nearshore, sheltered to offshore, exposed reef sites, but also varied over seasons. Comparing our data to other reef locations, calcification in the Red Sea was in the range of data collected from reefs in the Caribbean and Indo-Pacific; however, Acropora calcification estimates were at the lower end of worldwide rates. Our study shows that the increasing coral cover from nearshore to offshore environments aligned with CC calcification but not coral calcification, highlighting the potentially important role of CC in structuring reef cover and habitats. While coral calcification maxima have been typically observed during summer in many reef locations worldwide, calcification maxima during spring in the central Red Sea indicate that summer temperatures exceed the optima of reef calcifiers in this region. This study provides a foundation for comparative efforts and sets a baseline to quantify impact of future environmental change in the central Red Sea.
    • Stable mucus-associated bacterial communities in bleached and healthy corals of Porites lobata from the Arabian Seas

      Hadaidi, Ghaida; Röthig, Till; Yum, Lauren K.; Ziegler, Maren; Arif, Chatchanit; Roder, Cornelia; Burt, John; Voolstra, Christian R.; King Abdullah University of Science and Technology (KAUST); New York University, Abu Dhabi (Nature Research, 2017-03-31)
      Coral reefs are subject to coral bleaching manifested by the loss of endosymbiotic algae from coral host tissue. Besides algae, corals associate with bacteria. In particular, bacteria residing in the surface mucus layer are thought to mediate coral health, but their role in coral bleaching is unknown. We collected mucus from bleached and healthy Porites lobata colonies in the Persian/Arabian Gulf (PAG) and the Red Sea (RS) to investigate bacterial microbiome composition using 16S rRNA gene amplicon sequencing. We found that bacterial community structure was notably similar in bleached and healthy corals, and the most abundant bacterial taxa were identical. However, fine-scale differences in bacterial community composition between the PAG and RS were present and aligned with predicted differences in sulfur- and nitrogen-cycling processes. Based on our data, we argue that bleached corals benefit from the stable composition of mucus bacteria that resemble their healthy coral counterparts and presumably provide a conserved suite of protective functions, but monitoring of post-bleaching survival is needed to further confirm this assumption. Conversely, fine-scale site-specific differences highlight flexibility of the bacterial microbiome that may underlie adjustment to local environmental conditions and contribute to the widespread success of Porites lobata.
    • Transcriptomes and expression profiling of deep-sea corals from the Red Sea provide insight into the biology of azooxanthellate corals

      Yum, Lauren K.; Baumgarten, Sebastian; Röthig, Till; Roder, Cornelia; Roik, Anna; Michell, Craig; Voolstra, Christian R.; King Abdullah University of Science and Technology (KAUST) (Nature Research, 2017-07-25)
      Despite the importance of deep-sea corals, our current understanding of their ecology and evolutionis limited due to difficulties in sampling and studying deep-sea environments. Moreover, a recent reevaluation 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 provides direction for future research and further insight to organismal response of deep sea coral to environmental change and ocean warming.
    • Xestospongia testudinaria nighttime mass spawning observation in Indonesia.

      RÖTHIG, Till; VOOLSTRA, Christian R; King Abdullah University of Science and Technology (KAUST); Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology; Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology (The Japanese Coral Reef Society, 2016-10-13)