Rädecker, Nils
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Heat stress reduces the contribution of diazotrophs to coral holobiont nitrogen cycling
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.
Nutrient pollution enhances productivity and framework dissolution in algae- but not in coral-dominated reef communities
Ecosystem services provided by coral reefs may be susceptible to the combined effects of benthic species shifts and anthropogenic nutrient pollution, but related field studies are scarce. We thus investigated in situ how dissolved inorganic nutrient enrichment, maintained for two months, affected community-wide biogeochemical functions of intact coral- and degraded algae-dominated reef patches in the central Red Sea. Results from benthic chamber incubations revealed 87% increased gross productivity and a shift from net calcification to dissolution in algae-dominated communities after nutrient enrichment, but the same processes were unaffected by nutrients in neighboring coral communities. Both community types changed from net dissolved organic nitrogen sinks to sources, but the increase in net release was 56% higher in algae-dominated communities. Nutrient pollution may, thus, amplify the effects of community shifts on key ecosystem services of coral reefs, possibly leading to a loss of structurally complex habitats with carbonate dissolution and altered nutrient recycling.
Relative abundance of nitrogen cycling microbes in coral holobionts reflects environmental nitrate availability
Recent research suggests that nitrogen (N) cycling microbes are important for coral holobiont functioning. In particular, coral holobionts may acquire bioavailable N via prokaryotic dinitrogen (N2) fixation or remove excess N via denitrification activity. However, our understanding of environmental drivers on these processes in hospite remains limited. Employing the strong seasonality of the central Red Sea, this study assessed the effects of environmental parameters on the proportional abundances of N cycling microbes associated with the hard corals Acropora hemprichii and Stylophora pistillata. Specifically, we quantified changes in the relative ratio between nirS and nifH gene copy numbers, as a proxy for seasonal shifts in denitrification and N2 fixation potential in corals, respectively. In addition, we assessed coral tissue-associated Symbiodiniaceae cell densities and monitored environmental parameters to provide a holobiont and environmental context, respectively. While ratios of nirS to nifH gene copy numbers varied between seasons, they revealed similar seasonal patterns in both coral species, with ratios closely following patterns in environmental nitrate availability. Symbiodiniaceae cell densities aligned with environmental nitrate availability, suggesting that the seasonal shifts in nirS to nifH gene abundance ratios were probably driven by nitrate availability in the coral holobiont. Thereby, our results suggest that N cycling in coral holobionts probably adjusts to environmental conditions by increasing and/or decreasing denitrification and N2 fixation potential according to environmental nitrate availability. Microbial N cycling may, thus, extenuate the effects of changes in environmental nitrate availability on coral holobionts to support the maintenance of the coral–Symbiodiniaceae symbiosis.
Simultaneous Measurements of Dinitrogen Fixation and Denitrification Associated With Coral Reef Substrates : Advantages and Limitations of a Combined Acetylene Assay
Nitrogen (N) cycling in coral reefs is of key importance for these oligotrophic ecosystems, but knowledge about its pathways is limited. While dinitrogen (N2) fixation is comparably well studied, the counteracting denitrification pathway is under-investigated, mainly because of expensive and relatively complex experimental techniques currently available. Here, we combined two established acetylene-based assays to one single setup to determine N2-fixation and denitrification performed by microbes associated with coral reef substrates/organisms simultaneously. Accumulating target gases (ethylene for N2-fixation, nitrous oxide for denitrification) were measured in gaseous headspace samples via gas chromatography. We measured N2-fixation and denitrification rates of two Red Sea coral reef substrates (filamentous turf algae, coral rubble), and demonstrated, for the first time, the co-occurrence of both N-cycling processes in both substrates. N2-fixation rates were up to eight times higher during the light compared to the dark, whereas denitrification rates during dark incubations were stimulated for turf algae and suppressed for coral rubble compared to light incubations. Our results highlight the importance of both substrates in fixing N, but their role in relieving N is potentially divergent. Absolute N2-fixation rates of the present study correspond with rates reported previously, even though likely underestimated due to an initial lag phase. Denitrification is also presumably underestimated due to incomplete nitrous oxide inhibition and/or substrate limitation. Besides these inherent limitations, we show that a relative comparison of N2-fixation and denitrification activity between functional groups is possible. Thus, our approach facilitates cost-efficient sample processing in studies interested in comparing relative rates of N2-fixation and denitrification.
Nitrogen fixation and denitrification activity differ between coral- and algae-dominated Red Sea reefs
Coral reefs experience phase shifts from coral- to algae-dominated benthic communities, which could affect the interplay between processes introducing and removing bioavailable nitrogen. However, the magnitude of such processes, i.e., dinitrogen (N2) fixation and denitrification levels, and their responses to phase shifts remain unknown in coral reefs. We assessed both processes for the dominant species of six benthic categories (hard corals, soft corals, turf algae, coral rubble, biogenic rock, and reef sands) accounting for > 98% of the benthic cover of a central Red Sea coral reef. Rates were extrapolated to the relative benthic cover of the studied organisms in co-occurring coral- and algae-dominated areas of the same reef. In general, benthic categories with high N2 fixation exhibited low denitrification activity. Extrapolated to the respective reef area, turf algae and coral rubble accounted for > 90% of overall N2 fixation, whereas corals contributed to more than half of reef denitrification. Total N2 fixation was twice as high in algae- compared to coral-dominated areas, whereas denitrification levels were similar. We conclude that algae-dominated reefs promote new nitrogen input through enhanced N2 fixation and comparatively low denitrification. The subsequent increased nitrogen availability could support net productivity, resulting in a positive feedback loop that increases the competitive advantage of algae over corals in reefs that experienced a phase shift.
Heat stress destabilizes symbiotic nutrient cycling in corals
Recurrent mass bleaching events are pushing coral reefs worldwide to the brink of ecological collapse. While the symptoms and consequences of this breakdown of the coral-algal symbiosis have been extensively characterized, our understanding of the underlying causes remains incomplete. Here, we investigated the nutrient fluxes and the physiological as well as molecular responses of the widespread coral Stylophora pistillata to heat stress prior to the onset of bleaching to identify processes involved in the breakdown of the coral-algal symbiosis. We show that altered nutrient cycling during heat stress is a primary driver of the functional breakdown of the symbiosis. Heat stress increased the metabolic energy demand of the coral host, which was compensated by the catabolic degradation of amino acids. The resulting shift from net uptake to release of ammonium by the coral holobiont subsequently promoted the growth of algal symbionts and retention of photosynthates. Together, these processes form a feedback loop that will gradually lead to the decoupling of carbon translocation from the symbiont to the host. Energy limitation and altered symbiotic nutrient cycling are thus key factors in the early heat stress response, directly contributing to the breakdown of the coral-algal symbiosis. Interpreting the stability of the coral holobiont in light of its metabolic interactions provides a missing link in our understanding of the environmental drivers of bleaching and may ultimately help uncover fundamental processes underpinning the functioning of endosymbioses in general.
High rates of carbon and dinitrogen fixation suggest a critical role of benthic pioneer communities in the energy and nutrient dynamics of coral reefs
1. Following coral mortality in tropical reefs, pioneer communities dominated by filamentous and crustose algae efficiently colonize substrates previously occupied by coral tissue. This phenomenon is particularly common after mass coral mortality following prolonged bleaching events associated with marine heatwaves.
2. Pioneer communities play an important role for the biological succession and reorganization of reefs after disturbance. However, their significance for critical ecosystem functions previously mediated by corals, such as the efficient cycling of carbon (C) and nitrogen (N) within the reef, remains uncertain.
3. We used 96 carbonate tiles to simulate the occurrence of bare substrates after disturbance in a coral reef of the central Red Sea. We measured rates of C and dinitrogen (N2) fixation of pioneer communities on these tiles monthly over an entire year. Coupled with elemental and stable isotope analyses, these measurements provide insights into macronutrient acquisition, export and the influence of seasonality.
4. Pioneer communities exhibited high rates of C and N2 fixation within 4–8 weeks after the introduction of experimental bare substrates. Ranging from 13 to 25 μmol C cm−2 day−1 and 8 to 54 nmol N cm−2 day−1, respectively, C and N2 fixation rates were comparable to reported values for established Red Sea coral reefs. This similarity indicates that pioneer communities may quickly compensate for the loss of benthic productivity by corals. Notably, between 40% and 85% of fixed organic C was exported into the environment, constituting a vital source of energy for the coral reef food web.
5. Our findings suggest that benthic pioneer communities may play a crucial, yet overlooked role in the C and N dynamics of oligotrophic coral reefs by contributing to the input of new C and N after coral mortality. While not substituting other critical ecosystem functions provided by corals (e.g. structural habitat complexity and coastal protection), pioneer communities likely contribute to maintaining coral reef nutrient cycling through the accumulation of biomass and import of macronutrients following coral loss.
High plasticity of nitrogen fixation and denitrification of common coral reef substrates in response to nitrate availability
Nitrogen cycling in coral reefs may be affected by nutrient availability, but knowledge about concentration-dependent thresholds that modulate dinitrogen fixation and denitrification is missing. We determined the effects of different nitrate concentrations (ambient, 1, 5, 10 μM nitrate addition) on both processes under two light scenarios (i.e., light and dark) using a combined acetylene assay for two common benthic reef substrates, i.e., turf algae and coral rubble. For both substrates, dinitrogen fixation rates peaked at 5 μM nitrate addition in light, whereas denitrification was highest at 10 μM nitrate addition in the dark. At 10 μm nitrate addition in the dark, a near-complete collapse of dinitrogen fixation concurrent with a 76-fold increase in denitrification observed for coral rubble, suggesting potential threshold responses linked to the nutritional state of the community. We conclude that dynamic nitrogen cycling activity may help stabilise nitrogen availability in microbial communities associated with coral reef substrates.
High summer temperatures amplify functional differences between coral- and algae-dominated reef communities
Shifts from coral to algal dominance are expected to increase in tropical coral reefs as a result of anthropogenic disturbances. The consequences for key ecosystem functions such as primary productivity, calcification, and nutrient recycling are poorly understood, particularly under changing environmental conditions. We used a novel in situ incubation approach to compare functions of coral- and algae-dominated communities in the central Red Sea bi-monthly over an entire year. In situ gross and net community primary productivity, calcification, dissolved organic carbon fluxes, dissolved inorganic nitrogen fluxes, and their respective activation energies were quantified to describe the effects of seasonal changes. Overall, coral-dominated communities exhibited 30% lower net productivity and 10 times higher calcification than algae-dominated communities. Estimated activation energies indicated a higher thermal sensitivity of coral-dominated communities. In these communities, net productivity and calcification were negatively correlated with temperature (>40% and >65% reduction, respectively, with +5°C increase from winter to summer), while carbon losses via respiration and dissolved organic carbon release were more than doubled at higher temperatures. In contrast, algae-dominated communities doubled net productivity in summer, while calcification and dissolved organic carbon fluxes were unaffected. These results suggest pronounced changes in community functioning associated with phase shifts. Algae-dominated communities may outcompete coral-dominated communities due to their higher productivity and carbon retention to support fast biomass accumulation while compromising the formation of important reef framework structures. Higher temperatures likely amplify these functional differences, indicating a high vulnerability of ecosystem functions of coral-dominated communities to temperatures even below coral bleaching thresholds. Our results suggest that ocean warming may not only cause but also amplify coral-algal phase shifts in coral reefs.
In situ eutrophication stimulates dinitrogen fixation, denitrification, and productivity in Red Sea coral reefs
Eutrophication (i.e. the increase of [in-]organic nutrients) may affect the functioning of coral reefs, but knowledge about the effects on nitrogen (N) cycling and its relationship to productivity within benthic reef communities is scarce. Thus, we investigated how in situ manipulated eutrophication impacted productivity along with 2 counteracting N-cycling pathways (dinitrogen [N2]-fixation, denitrification), using a combined acetylene assay. We hypothesised that N2-fixation would decrease and denitrification increase in response to eutrophication. N fluxes and productivity (measured as dark and light oxygen fluxes assessed in incubation experiments) were determined for 3 dominant coral reef functional groups (reef sediments, turf algae, and the scleractinian coral Pocillopora verrucosa) after 8 wk of in situ nutrient enrichment in the central Red Sea. Using slow-release fertiliser, we increased the dissolved inorganic N concentration by up to 7-fold compared to ambient concentrations. Experimental nutrient enrichment stimulated both N2-fixation and denitrification across all functional groups 2- to 7-fold and 2- to 4-fold, respectively. Productivity doubled in reef sediments and remained stable for turf algae and P. verrucosa. Our data therefore suggest that (1) turf algae are major N2-fixers in coral reefs, while denitrification is widespread among all investigated groups; (2) surprisingly, and contrary to our hypothesis, both N2-fixation and denitrification are involved in the response to moderate N eutrophication, and (3) stimulated N2-fixation and denitrification are not directly influenced by productivity. Our findings underline the importance and ubiquity of microbial N cycling in (Red Sea) coral reefs along with its sensitivity to eutrophication.