Ocean warming threatens corals and the coral reef ecosystem. Nevertheless, corals can be adapted to their thermal environment and inherit heat tolerance across generations. In addition, the diverse ...microbes that associate with corals have the capacity for more rapid change, potentially aiding the adaptation of long-lived corals. Here, we show that the microbiome of reef corals is different across thermally variable habitats and changes over time when corals are reciprocally transplanted. Exposing these corals to thermal bleaching conditions changes the microbiome for heat-sensitive corals, but not for heat-tolerant corals growing in habitats with natural high heat extremes. Importantly, particular bacterial taxa predict the coral host response in a short-term heat stress experiment. Such associations could result from parallel responses of the coral and the microbial community to living at high natural temperatures. A competing hypothesis is that the microbial community and coral heat tolerance are causally linked.
The association between corals and photosynthetic dinoflagellates (Symbiodinium spp.) is the key to the success of reef ecosystems in highly oligotrophic environments, but it is also their Achilles' ...heel due to its vulnerability to local stressors and the effects of climate change. Research during the last two decades has shaped a view that coral host-Symbiodinium pairings are diverse, but largely exclusive. Deep sequencing has now revealed the existence of a rare diversity of cryptic Symbiodinium assemblages within the coral holobiont, in addition to one or a few abundant algal members. While the contribution of the most abundant resident Symbiodinium species to coral physiology is widely recognized, the significance of the rare and low abundant background Symbiodinium remains a matter of debate. In this study, we assessed how coral-Symbiodinium communities assemble and how rare and abundant components together constitute the Symbiodinium community by analyzing 892 coral samples comprising >110 000 unique Symbiodinium ITS2 marker gene sequences. Using network modeling, we show that host-Symbiodinium communities assemble in non-random 'clusters' of abundant and rare symbionts. Symbiodinium community structure follows the same principles as bacterial communities, for which the functional significance of rare members (the 'rare bacterial biosphere') has long been recognized. Importantly, the inclusion of rare Symbiodinium taxa in robustness analyses revealed a significant contribution to the stability of the host-symbiont community overall. As such, it highlights the potential functions rare symbionts may provide to environmental resilience of the coral holobiont.
The global decline of coral reefs heightens the need to understand how corals respond to changing environmental conditions. Corals are metaorganisms, so-called holobionts, and restructuring of the ...associated bacterial community has been suggested as a means of holobiont adaptation. However, the potential for restructuring of bacterial communities across coral species in different environments has not been systematically investigated. Here we show that bacterial community structure responds in a coral host-specific manner upon cross-transplantation between reef sites with differing levels of anthropogenic impact. The coral Acropora hemprichii harbors a highly flexible microbiome that differs between each level of anthropogenic impact to which the corals had been transplanted. In contrast, the microbiome of the coral Pocillopora verrucosa remains remarkably stable. Interestingly, upon cross-transplantation to unaffected sites, we find that microbiomes become indistinguishable from back-transplanted controls, suggesting the ability of microbiomes to recover. It remains unclear whether differences to associate with bacteria flexibly reflects different holobiont adaptation mechanisms to respond to environmental change.
Coral bleaching, caused by the loss of brownish-colored dinoflagellate photosymbionts from the host tissue of reef-building corals, is a major threat to reef survival. Occasionally, bleached corals ...become exceptionally colorful rather than white. These colors derive from photoprotective green fluorescent protein (GFP)-like pigments produced by the coral host. There is currently no consensus regarding what causes colorful bleaching events and what the consequences for the corals are. Here, we document that colorful bleaching events are a recurring phenomenon in reef regions around the globe. Our analysis of temperature conditions associated with colorful bleaching events suggests that corals develop extreme coloration within 2 to 3 weeks after exposure to mild or temporary heat stress. We demonstrate that the increase of light fluxes in symbiont-depleted tissue promoted by reflection of the incident light from the coral skeleton induces strong expression of the photoprotective coral host pigments. We describe an optical feedback loop involving both partners of the association, discussing that the mitigation of light stress offered by host pigments could facilitate recolonization of bleached tissue by symbionts. Our data indicate that colorful bleaching has the potential to identify local environmental factors, such as nutrient stress, that can exacerbate the impact of elevated temperatures on corals, to indicate the severity of heat stress experienced by corals and to gauge their post-stress recovery potential.
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•Colorful bleaching is a recurring phenomenon in reef regions around the globe•Colors result from blue-light-driven host pigment upregulation following bleaching•Photoprotective host pigments in bleached tissue can aid symbiont recolonization•Colorful bleaching can be indicative of brief or mild heat and/or nutrient stress
Bollati et al. document the global incidence of colorful bleaching events and describe the physiological mechanism behind the striking phenomenon. Extreme colors result from upregulation of photoprotective host pigments driven by increased internal light fluxes following symbiont loss.
We present SymPortal (SymPortal.org), a novel analytical framework and platform for genetically resolving the algal symbionts of reef corals using next‐generation sequencing (NGS) data of the ITS2 ...rDNA. Although the ITS2 marker is widely used to genetically characterize taxa within the family Symbiodiniaceae (formerly the genus Symbiodinium), the multicopy nature of the marker complicates its use. Commonly, the intragenomic diversity resultant from this multicopy nature is collapsed by analytical approaches, thereby focusing on only the most abundant sequences. In contrast, SymPortal employs logic to identify within‐sample informative intragenomic sequences, which we have termed ‘defining intragenomic variants' (DIVs), to identify ITS2‐type profiles representative of putative Symbiodiniaceae taxa. By making use of this intragenomic ITS2 diversity, SymPortal is able to resolve genetic delineations using the ITS2 marker at a level that was previously only possible by using additional genetic markers. We demonstrate this by comparing this novel approach to the most commonly used alternative approach for NGS ITS2 data, the 97% similarity clustering to operational taxonomic units (OTUs). The SymPortal platform accepts NGS raw sequencing data as input to provide an easy‐to‐use, standardization‐enforced, and community‐driven framework that integrates with a database to gain resolving power with increased use. We consider that SymPortal, in conjunction with ongoing large‐scale sampling and sequencing efforts, should play an instrumental role in making future sampling efforts more comparable and in maximizing their efficacy in working towards the classification of the global Symbiodiniaceae diversity.
Tropical reefs have been impacted by thermal anomalies caused by global warming that induced coral bleaching and mortality events globally. However, there have only been very few recordings of ...bleaching within the Red Sea despite covering a latitudinal range of 15° and consequently it has been considered a region that is less sensitive to thermal anomalies. We therefore examined historical patterns of sea surface temperature (SST) and associated anomalies (1982–2012) and compared warming trends with a unique compilation of corresponding coral bleaching records from throughout the region. These data indicated that the northern Red Sea has not experienced mass bleaching despite intensive Degree Heating Weeks (DHW) of >15°C‐weeks. Severe bleaching was restricted to the central and southern Red Sea where DHWs have been more frequent, but far less intense (DHWs <4°C‐weeks). A similar pattern was observed during the 2015–2016 El Niño event during which time corals in the northern Red Sea did not bleach despite high thermal stress (i.e. DHWs >8°C‐weeks), and bleaching was restricted to the central and southern Red Sea despite the lower thermal stress (DHWs < 8°C‐weeks). Heat stress assays carried out in the northern (Hurghada) and central (Thuwal) Red Sea on four key reef‐building species confirmed different regional thermal susceptibility, and that central Red Sea corals are more sensitive to thermal anomalies as compared to those from the north. Together, our data demonstrate that corals in the northern Red Sea have a much higher heat tolerance than their prevailing temperature regime would suggest. In contrast, corals from the central Red Sea are close to their thermal limits, which closely match the maximum annual water temperatures. The northern Red Sea harbours reef‐building corals that live well below their bleaching thresholds and thus we propose that the region represents a thermal refuge of global importance.
(1) Tropical reefs have been impacted by thermal anomalies that have induced coral bleaching; however, there are only few recordings of bleaching across the Red Sea. (2) Historical and contemporary mass bleaching appears to be restricted to the central and southern Red Sea, and the northern region remains bleaching‐free despite experiencing intensive thermal anomalies. (3) Heat stress experiments demonstrated that corals in the north are thermally tolerant and exist within a region where ambient and anomalous temperatures are lower than their physiological thermal maximum and we therefore propose that the northern region is thermal refugia with global significance.
Aim: Coral reefs rely on the symbiosis between scleractinian corals and intracellular, photosynthetic dinoflagellates of the genus Symbiodinium making the assessment of symbiont diversity critical to ...our understanding of ecological resilience of these ecosystems. This study characterizes Symbiodinium diversity around the Arabian Peninsula, which contains some of the most thermally diverse and understudied reefs on Earth. Location: Shallow water coral reefs throughout the Red Sea (RS), Sea of Oman (SO), and Persian/Arabian Gulf (PAG). Methods: Next-generation sequencing of the ITS2 marker gene was used to assess Symbiodinium community composition and diversity comprising 892 samples from 46 hard and soft coral genera. Results: Corals were associated with a large diversity of Symbiodinium, which usually consisted of one or two prevalent symbiont types and many types at low abundance. Symbiodinium communities were strongly structured according to geographical region and to a lesser extent by coral host identity. Overall symbiont communities were composed primarily of species from dade A and C in the RS, clade A, C, and D in the SO, and clade C and D in the PAG, representing a gradual shift from C- to D-dominated coral hosts. The analysis of symbiont diversity in an Operational Taxonomic Unit (OTU)-based framework allowed the identification of differences in symbiont taxon richness over geographical regions and host genera. Main conclusions: Our study represents a comprehensive overview over biogeography and molecular diversity of Symbiodinium in the Arabian Seas, where coral reefs thrive in one of the most extreme environmental settings on the planet. As such our data will serve as a baseline for further exploration into the effects of environmental change on host-symbiont pairings and the identification and ecological significance of Symbiodinium types from regions already experiencing ' Future Ocean' conditions.
Deserts, such as those found in Saudi Arabia, are one of the most hostile places for plant growth. However, desert plants are able to impact their surrounding microbial community and select ...beneficial microbes that promote their growth under these extreme conditions. In this study, we examined the soil, rhizosphere and endosphere bacterial communities of four native desert plants Tribulus terrestris, Zygophyllum simplex, Panicum turgidum and Euphorbia granulata from the Southwest (Jizan region), two of which were also found in the Midwest (Al Wahbah area) of Saudi Arabia. While the rhizosphere bacterial community mostly resembled that of the highly different surrounding soils, the endosphere composition was strongly correlated with its host plant phylogeny. In order to assess whether any of the native bacterial endophytes might have a role in plant growth under extreme conditions, we analyzed the properties of 116 cultured bacterial isolates that represent members of the phyla Proteobacteria, Bacteroidetes, Actinobacteria and Firmicutes. Our analysis shows that different strains have highly different biochemical properties with respect to nutrient acquisition, hormone production and growth under stress conditions. More importantly, eleven of the isolated strains could confer salinity stress tolerance to the experimental model plant Arabidopsis thaliana suggesting some of these plant-associated bacteria might be useful for improving crop desert agriculture.
The pollution of the marine environment with microplastics is pervasive. However, microplastic concentrations in the seawater are lower than the number of particles entering the oceans, suggesting ...that plastic particles accumulate in environmental sinks. Yet, the exact long‐term sinks related to the “missing plastic” phenomenon are barely explored. Sediments in nearshore biogenic habitats are known to trap large amounts of microplastics, but also the three‐dimensional structures of coral reefs might serve as unique, living long‐term sinks. The main framework builders, reef‐building corals, have been shown to ingest and overgrow microplastics, potentially leading to a deposition of particles in reef structures. However, little is known about the number of deposited particles and the underlying processes determining the permanent deposition in the coral skeletons. To test whether corals may act as living long‐term sink for microplastic, we exposed four reef‐building coral species to polyethylene microplastics (200 particles L−1) in an 18‐month laboratory experiment. We found microplastics in all treatment specimens, with low numbers of particles trapped in the coral tissue (up to 2 particles per cm2) and much higher numbers in the skeleton (up to 84 particles per cm3). The numbers of particles accumulated in the coral skeletons were mainly related to coral growth (i.e., skeletal growth in volume), suggesting that deposition is a regularly occurring stochastic process. We estimate that reef‐building corals may remove 0.09%–2.82% of the bioavailable microplastics from tropical shallow‐reef waters per year. Our study shows for the first time that microplastic particles accumulate permanently in a biological sink, helping to explain the “missing plastic” phenomenon. This highlights the importance of coral reefs for the ecological balance of the oceans and reinforces the need to protect them, not only to mitigate the effects of climate change but also to preserve their ecosystem services as long‐term sink for microplastic.
To investigate whether tropical shallow‐water reef‐building corals can act as long‐term sinks for microplastics, we exposed four common reef‐building coral species to polyethylene microplastics for 18 months in a microcosm experiment. We found that reef‐building corals permanently incorporate microplastics into their skeletons, acting as unique biological sink for microplastics. We estimate that tropical reef‐building corals worldwide can accumulate ~1% of the particles present in tropical reef waters annually and represent a previously unknown link in the “missing plastic” phenomenon.
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.
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