Molecular insights into the Darwin paradox of coral reefs from the sea anemone Aiptasia
2023-03-17, Cui, Guoxin, Konciute, Migle K., Ling, Lorraine, Esau, Luke, Raina, Jean-Baptiste, Han, Baoda, Salazar, Octavio R., Rädecker, Nils, Voolstra, Christian R., Aranda, Manuel
Symbiotic cnidarians such as corals and anemones form highly productive and biodiverse coral reef ecosystems in nutrient-poor ocean environments, a phenomenon known as Darwin’s paradox. Resolving this paradox requires elucidating the molecular bases of efficient nutrient distribution and recycling in the cnidarian-dinoflagellate symbiosis. Using the sea anemone Aiptasia, we show that during symbiosis, the increased availability of glucose and the presence of the algae jointly induce the coordinated up-regulation and relocalization of glucose and ammonium transporters. These molecular responses are critical to support symbiont functioning and organism-wide nitrogen assimilation through glutamine synthetase/glutamate synthase–mediated amino acid biosynthesis. Our results reveal crucial aspects of the molecular mechanisms underlying nitrogen conservation and recycling in these organisms that allow them to thrive in the nitrogen-poor ocean environments.
Greater functional diversity and redundancy of coral endolithic microbiomes align with lower coral bleaching susceptibility
2022-10, Cárdenas, Anny, Raina, Jean-Baptiste, Pogoreutz, Claudia, Rädecker, Nils, Bougoure, Jeremy, Guagliardo, Paul, Pernice, Mathieu, Voolstra, Christian R.
The skeleton of reef-building coral harbors diverse microbial communities that could compensate for metabolic deficiencies caused by the loss of algal endosymbionts, i.e., coral bleaching. However, it is unknown to what extent endolith taxonomic diversity and functional potential might contribute to thermal resilience. Here we exposed Goniastrea edwardsi and Porites lutea, two common reef-building corals from the central Red Sea to a 17-day long heat stress. Using hyperspectral imaging, marker gene/metagenomic sequencing, and NanoSIMS, we characterized their endolithic microbiomes together with 15N and 13C assimilation of two skeletal compartments: the endolithic band directly below the coral tissue and the deep skeleton. The bleaching-resistant G. edwardsi was associated with endolithic microbiomes of greater functional diversity and redundancy that exhibited lower N and C assimilation than endoliths in the bleaching-sensitive P. lutea. We propose that the lower endolithic primary productivity in G. edwardsi can be attributed to the dominance of chemolithotrophs. Lower primary production within the skeleton may prevent unbalanced nutrient fluxes to coral tissues under heat stress, thereby preserving nutrient-limiting conditions characteristic of a stable coral-algal symbiosis. Our findings link coral endolithic microbiome structure and function to bleaching susceptibility, providing new avenues for understanding and eventually mitigating reef loss.
Heat stress reduces the contribution of diazotrophs to coral holobiont nitrogen cycling
2022-04, Rädecker, Nils, Pogoreutz, Claudia, Gegner, Hagen M., Cárdenas, Anny, Perna, Gabriela, Geißler, Laura, Roth, Florian, Bougoure, Jeremy, Guagliardo, Paul, Voolstra, Christian R.
Efficient nutrient cycling in the coral-algal symbiosis requires constant but limited nitrogen availability. Coral-associated diazotrophs, i.e., prokaryotes capable of fixing dinitrogen, may thus support productivity in a stable coral-algal symbiosis but could contribute to its breakdown when overstimulated. However, the effects of environmental conditions on diazotroph communities and their interaction with other members of the coral holobiont remain poorly understood. Here we assessed the effects of heat stress on diazotroph diversity and their contribution to holobiont nutrient cycling in the reef-building coral Stylophora pistillata from the central Red Sea. In a stable symbiotic state, we found that nitrogen fixation by coral-associated diazotrophs constitutes a source of nitrogen to the algal symbionts. Heat stress caused an increase in nitrogen fixation concomitant with a change in diazotroph communities. Yet, this additional fixed nitrogen was not assimilated by the coral tissue or the algal symbionts. We conclude that although diazotrophs may support coral holobiont functioning under low nitrogen availability, altered nutrient cycling during heat stress abates the dependence of the coral host and its algal symbionts on diazotroph-derived nitrogen. Consequently, the role of nitrogen fixation in the coral holobiont is strongly dependent on its nutritional status and varies dynamically with environmental conditions.
Microbes support enhanced nitrogen requirements of coral holobionts in a high CO2 environment
2021-11, Meunier, Valentine, Geißler, Laura, Bonnet, Sophie, Rädecker, Nils, Perna, Gabriela, Grosso, Olivier, Lambert, Christophe, Rodolfo-Metalpa, Riccardo, Voolstra, Christian R., Houlbrèque, Fanny
Ocean acidification is posing a threat to calcifying organisms due to the increased energy requirements of calcification under high CO2 conditions. The ability of scleractinian corals to cope with future ocean conditions will thus depend on their ability to fulfill their carbon requirement. However, the primary productivity of coral holobionts is limited by low nitrogen (N) availability in coral reef waters. Here, we employed CO2 seeps of Tutum Bay (Papua New Guinea) as a natural laboratory to understand how coral holobionts offset their increased energy requirements under high CO2 conditions. Our results demonstrate for the first time that under high pCO2 conditions, N assimilation pathways of Pocillopora damicornis are jointly modified. We found that diazotroph-derived N assimilation rates in the Symbiodiniaceae were significantly higher in comparison to an ambient CO2 control site, concomitant with a restructured diazotroph community and the specific prevalence of an alpha-proteobacterium. Further, corals at the high CO2 site also had increased feeding rates on picoplankton and in particular exhibited selective feeding on Synechococcus sp., known to be rich in N. Given the high abundance of picoplankton in oligotrophic waters at large, our results suggest that corals exhibiting flexible diazotrophic communities and capable of exploiting N-rich picoplankton sources to offset their increased N requirements may be able to cope better in a high pCO2 world.
Excess labile carbon promotes diazotroph abundance in heat-stressed octocorals
2023-03, Xiang, Nan, Meyer, Achim, Pogoreutz, Claudia, Rädecker, Nils, Voolstra, Christian R., Wild, Christian, Gärdes, Astrid
Nitrogen limitation is the foundation of stable coral-algal symbioses. Diazotrophs, prokaryotes capable of fixing N 2 into ammonia, support the productivity of corals in oligotrophic waters, but could contribute to the destabilization of holobiont functioning when overstimulated. Recent studies on reef-building corals have shown that labile dissolved organic carbon (DOC) enrichment or heat stress increases diazotroph abundance and activity, thereby increasing nitrogen availability and destabilizing the coral-algal symbiosis. However, the (a)biotic drivers of diazotrophs in octocorals are still poorly understood. We investigated diazotroph abundance (via relative quantification of nifH gene copy numbers) in two symbiotic octocorals, the more mixotrophic soft coral Xenia umbellata and the more autotrophic gorgonian Pinnigorgia flava, under (i) labile DOC enrichment for 21 days, followed by (ii) combined labile DOC enrichment and heat stress for 24 days. Without heat stress, relative diazotroph abundances in X. umbellata and P. flava were unaffected by DOC enrichment. During heat stress, DOC enrichment (20 and 40 mg glucose l −1 ) increased the relative abundances of diazotrophs by sixfold in X. umbellata and fourfold in P. flava , compared with their counterparts without excess DOC. Our data suggest that labile DOC enrichment and concomitant heat stress could disrupt the nitrogen limitation in octocorals by stimulating diazotroph proliferation. Ultimately, the disruption of nitrogen cycling may further compromise octocoral fitness by destabilizing symbiotic nutrient cycling. Therefore, improving local wastewater facilities to reduce labile DOC input into vulnerable coastal ecosystems may help octocorals cope with ocean warming.
Coral holobiont cues prime Endozoicomonas for a symbiotic lifestyle
2022-08, Pogoreutz, Claudia, Oakley, Clinton A., Rädecker, Nils, Cárdenas, Anny, Perna, Gabriela, Xiang, Nan, Peng, Lifeng, Davy, Simon K., Ngugi, David K., Voolstra, Christian R.
Endozoicomonas are prevalent, abundant bacterial associates of marine animals, including corals. Their role in holobiont health and functioning, however, remains poorly understood. To identify potential interactions within the coral holobiont, we characterized the novel isolate Endozoicomonas marisrubri sp. nov. 6c and assessed its transcriptomic and proteomic response to tissue extracts of its native host, the Red Sea coral Acropora humilis. We show that coral tissue extracts stimulated differential expression of genes putatively involved in symbiosis establishment via the modulation of the host immune response by E. marisrubri 6c, such as genes for flagellar assembly, ankyrins, ephrins, and serpins. Proteome analyses revealed that E. marisrubri 6c upregulated vitamin B1 and B6 biosynthesis and glycolytic processes in response to holobiont cues. Our results suggest that the priming of Endozoicomonas for a symbiotic lifestyle involves the modulation of host immunity and the exchange of essential metabolites with other holobiont members. Consequently, Endozoicomonas may play an important role in holobiont nutrient cycling and may therefore contribute to coral health, acclimatization, and adaptation.
Projecting coral responses to intensifying marine heatwaves under ocean acidification
2022-03, Klein, Shannon G., Geraldi, Nathan R., Anton, Andrea, Schmidt-Roach, Sebastian, Ziegler, Maren, Cziesielski, Maha J., Martin, Cecilia, Rädecker, Nils, Frölicher, Thomas L., Voolstra, Christian R.
Over this century, coral reefs will run the gauntlet of climate change, as marine heatwaves (MHWs) become more intense and frequent, and ocean acidification (OA) progresses. However, we still lack a quantitative assessment of how, and to what degree, OA will moderate the responses of corals to MHWs as they intensify throughout this century. Here, we first projected future MHW intensities for tropical regions under three future greenhouse gas emissions scenario (representative concentration pathways, RCP2.6, RCP4.5 and RCP8.5) for the near-term (2021-2040), mid-century (2041-2060) and late-century (2081-2100). We then combined these MHW intensity projections with a global data set of 1,788 experiments to assess coral attribute performance and survival under the three emissions scenarios for the near-term, mid-century and late-century in the presence and absence of OA. Although warming and OA had predominately additive impacts on the coral responses, the contribution of OA in affecting most coral attributes was minor relative to the dominant role of intensifying MHWs. However, the addition of OA led to greater decreases in photosynthesis and survival under intermediate and unrestricted emissions scenario for the mid- and late-century than if intensifying MHWs were considered as the only driver. These results show that role of OA in modulating coral responses to intensifying MHWs depended on the focal coral attribute and extremity of the scenario examined. Specifically, intensifying MHWs and OA will cause increasing instances of coral bleaching and substantial declines in coral productivity, calcification and survival within the next two decades under the low and intermediate emissions scenario. These projections suggest that corals must rapidly adapt or acclimatize to projected ocean conditions to persist, which is far more likely under a low emissions scenario and with increasing efforts to manage reefs to enhance resilience.
Presence of algal symbionts affects denitrifying bacterial communities in the sea anemone Aiptasia coral model
2022-12, Xiang, Nan, Rädecker, Nils, Pogoreutz, Claudia, Cárdenas, Anny, Meibom, Anders, Wild, Christian, Gärdes, Astrid, Voolstra, Christian R.
The coral-algal symbiosis is maintained by a constant and limited nitrogen availability in the holobiont. Denitrifiers, i.e., prokaryotes reducing nitrate/nitrite to dinitrogen, could contribute to maintaining the nitrogen limitation in the coral holobiont, however the effect of host and algal identity on their community is still unknown. Using the coral model Aiptasia, we quantified and characterized the denitrifier community in a full-factorial design combining two hosts (CC7 and H2) and two strains of algal symbionts of the family Symbiodiniaceae (SSA01 and SSB01). Strikingly, relative abundance of denitrifiers increased by up to 22-fold in photosymbiotic Aiptasia compared to their aposymbiotic (i.e., algal-depleted) counterparts. In line with this, while the denitrifier community in aposymbiotic Aiptasia was largely dominated by diet-associated Halomonas, we observed an increasing relative abundance of an unclassified bacterium in photosymbiotic CC7, and Ketobacter in photosymbiotic H2, respectively. Pronounced changes in denitrifier communities of Aiptasia with Symbiodinium linucheae strain SSA01 aligned with the higher photosynthetic carbon availability of these holobionts compared to Aiptasia with Breviolum minutum strain SSB01. Our results reveal that the presence of algal symbionts increases abundance and alters community structure of denitrifiers in Aiptasia. Thereby, patterns in denitrifier community likely reflect the nutritional status of aposymbiotic vs. symbiotic holobionts. Such a passive regulation of denitrifiers may contribute to maintaining the nitrogen limitation required for the functioning of the cnidarian-algal symbiosis.
High light quantity suppresses locomotion in symbiotic Aiptasia
2022-05-27, Strumpen, Nils F., Rädecker, Nils, Pogoreutz, Claudia, Meibom, Anders, Voolstra, Christian R.
Many cnidarians engage in endosymbioses with microalgae of the family Symbiodiniaceae. In this association, the fitness of the cnidarian host is closely linked to the photosynthetic performance of its microalgal symbionts. Phototaxis may enable semi-sessile cnidarians to optimize the light regime for their microalgal symbionts. Indeed, phototaxis and phototropism have been reported in the photosymbiotic sea anemone Aiptasia. However, the influence of light quantity on the locomotive behavior of Aiptasia remains unknown. Here we show that light quantity and the presence of microalgal symbionts modulate the phototactic behavior in Aiptasia. Although photosymbiotic Aiptasia were observed to move in seemingly random directions along an experimental light gradient, their probability of locomotion depended on light quantity. As photosymbiotic animals were highly mobile in low light but almost immobile at high light quantities, photosymbiotic Aiptasia at low light quantities exhibited an effective net movement towards light levels sufficient for positive net photosynthesis. In contrast, aposymbiotic Aiptasia exhibited greater mobility than their photosymbiotic counterparts, regardless of light quantity. Our results suggest that photosynthetic activity of the microalgal symbionts suppresses locomotion in Aiptasia, likely by supporting a positive energy balance in the host. We propose that motile photosymbiotic organisms can develop phototactic behavior as a consequence of starvation linked to symbiotic nutrient cycling.
Contrasting Microbiome Dynamics of Putative Denitrifying Bacteria in Two Octocoral Species Exposed to Dissolved Organic Carbon (DOC) and Warming
2022-01-25, Xiang, Nan, Hassenrück, Christiane, Pogoreutz, Claudia, Rädecker, Nils, Simancas-Giraldo, Susana Marcela, Voolstra, Christian R., Wild, Christian, Gärdes, Astrid
Mutualistic nutrient cycling in the coral-algae symbiosis depends on limited nitrogen (N) availability for algal symbionts. Denitrifying prokaryotes capable of reducing nitrate or nitrite to dinitrogen could thus support coral holobiont functioning by limiting N availability. Octocorals show some of the highest denitrification rates among reef organisms; however, little is known about the community structures of associated denitrifiers and their response to environmental fluctuations. Combining 16S rRNA gene amplicon sequencing with nirS in-silico PCR and quantitative PCR, we found differences in bacterial community dynamics between two octocorals exposed to excess dissolved organic carbon (DOC) and concomitant warming. Although bacterial communities of the gorgonian Pinnigorgia flava remained largely unaffected by DOC and warming, the soft coral Xenia umbellata exhibited a pronounced shift toward Alphaproteobacteria dominance under excess DOC. Likewise, the relative abundance of denitrifiers was not altered in P. flava but decreased by 1 order of magnitude in X. umbellata under excess DOC, likely due to decreased proportions of Ruegeria spp. Given that holobiont C:N ratios remained stable in P. flava but showed a pronounced increase with excess DOC in X. umbellata, our results suggest that microbial community dynamics may reflect the nutritional status of the holobiont. Hence, denitrifier abundance may be directly linked to N availability. This suggests a passive regulation of N cycling microbes based on N availability, which could help stabilize nutrient limitation in the coral-algal symbiosis and thereby support holobiont functioning in a changing environment. IMPORTANCE Octocorals are important members of reef-associated benthic communities that can rapidly replace scleractinian corals as the dominant ecosystem engineers on degraded reefs. Considering the substantial change in the (a)biotic environment that is commonly driving reef degradation, maintaining a dynamic and metabolically diverse microbial community might contribute to octocoral acclimatization. Nitrogen (N) cycling microbes, in particular denitrifying prokaryotes, may support holobiont functioning by limiting internal N availability, but little is known about the identity and (a)biotic drivers of octocoral-associated denitrifiers. Here, we show contrasting dynamics of bacterial communities associated with two common octocoral species, the soft coral Xenia umbellata and the gorgonian Pinnigorgia flava after a 6-week exposure to excess dissolved organic carbon under concomitant warming conditions. The specific responses of denitrifier communities of the two octocoral species aligned with the nutritional status of holobiont members. This suggests a passive regulation based on N availability in the coral holobiont.