Rädecker, Nils
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Denitrification Aligns with N2 Fixation in Red Sea Corals
Denitrification may potentially alleviate excess nitrogen (N) availability in coral holobionts to maintain a favourable N to phosphorous ratio in the coral tissue. However, little is known about the abundance and activity of denitrifiers in the coral holobiont. The present study used the nirS marker gene as a proxy for denitrification potential along with measurements of denitrification rates in a comparative coral taxonomic framework from the Red Sea: Acropora hemprichii, Millepora dichotoma, and Pleuractis granulosa. Relative nirS gene copy numbers associated with the tissues of these common corals were assessed and compared with denitrification rates on the holobiont level. In addition, dinitrogen (N2) fixation rates, Symbiodiniaceae cell density, and oxygen evolution were assessed to provide an environmental context for denitrification. We found that relative abundances of the nirS gene were 16- and 17-fold higher in A. hemprichii compared to M. dichotoma and P. granulosa, respectively. In concordance, highest denitrification rates were measured in A. hemprichii, followed by M. dichotoma and P. granulosa. Denitrification rates were positively correlated with N2 fixation rates and Symbiodiniaceae cell densities. Our results suggest that denitrification may counterbalance the N input from N2 fixation in the coral holobiont, and we hypothesize that these processes may be limited by photosynthates released by the Symbiodiniaceae.
An in situ approach for measuring biogeochemical fluxes in structurally complex benthic communities
1. The exchange of energy and nutrients are integral components of ecological functions of benthic shallow‐water ecosystems and are directly dependent on in situ environmental conditions. Traditional laboratory experiments cannot account for the multidimensionality of interacting processes when assessing metabolic rates and biogeochemical fluxes of structurally complex benthic communities. Current in situ chamber systems are expensive, limited in their functionality and the deployment is often restricted to planar habitats (e.g. sediments or seagrass meadows) only.
2. To overcome these constraints, we describe a protocol to build and use non‐invasive, cost‐effective and easy to handle in situ incubation chambers that provide reproducible measurements of biogeochemical processes in simple and structurally complex benthic shallow‐water communities. Photogrammetry tools account for the structural complexity of benthic communities, enabling to calculate accurate community fluxes. We tested the performance of the system in laboratory assays and various benthic habitats (i.e. algae growing on rock, coral assemblages, sediments and seagrass meadows). In addition, we estimated community budgets of photosynthesis and respiration by corals, rock with algae and carbonate sediments, which were subsequently compared to budgets extrapolated from conventional ex situ single‐organism incubations.
3. The tests highlight the transparency (>90% light transmission) of the chambers and minimal water exchange with the surrounding medium on most substrates. Linear dissolved oxygen fluxes in dependence to incubation time showed sufficient mixing of the water by circulation pumps and no organismal stress response. The comparison to single‐organism incubations showed that ex situ measurements might overestimate community‐wide net primary production and underestimate respiration and gross photosynthesis by 20%–90%.
4. The proposed protocol overcomes the paucity of observational and manipulative studies that can be performed in in situ native habitats, thus producing widely applicable and realistic assessments on the community level. Importantly, the tool provides a standardized approach to compare community functions across a wide range of benthic habitats. We identify multiple experimental strategies, including the manipulation of stressors/factors, and discuss how the method may be implemented in a variety of aquatic studies.
Stimulated Respiration and Net Photosynthesis in Cassiopeia sp. during Glucose Enrichment Suggests in hospite CO2 Limitation of Algal Endosymbionts
The endosymbiosis between cnidarians and dinoflagellates of the genus Symbiodinium is key to the high productivity of tropical coral reefs. In this endosymbiosis, Symbiodinium translocate most of their photosynthates to their animal host in exchange for inorganic nutrients. Among these, carbon dioxide (CO2) derived from host respiration helps to meet the carbon requirements to sustain photosynthesis of the dinoflagellates. Nonetheless, recent studies suggest that productivity in symbiotic cnidarians such as corals is CO2-limited. Here we show that glucose enrichment stimulates respiration and gross photosynthesis rates by 80 and 140%, respectively, in the symbiotic upside-down jellyfish Cassiopeia sp. from the Central Red Sea. Our findings show that glucose was rapidly consumed and respired within the Cassiopeia sp. holobiont. The resulting increase of CO2 availability in hospite in turn likely stimulated photosynthesis in Symbiodinium. Hence, the increase of photosynthesis under these conditions suggests that CO2 limitation of Symbiodinium is a common feature of stable cnidarian holobionts and that the stimulation of holobiont metabolism may attenuate this CO2 limitation.
Nitrogen cycling in corals : the key to understanding holobiont functioning?
Corals are animals that form close mutualistic associations with endosymbiotic photosynthetic algae of the genus Symbiodinium. Together they provide the calcium carbonate framework of coral reef ecosystems. The importance of the microbiome (i.e., bacteria, archaea, fungi, and viruses) to holobiont functioning has only recently been recognized. Given that growth and density of Symbiodinium within the coral host is highly dependent on nitrogen availability, nitrogen-cycling microbes may be of fundamental importance to the stability of the coral-algae symbiosis and holobiont functioning, in particular under nutrient-enriched and -depleted scenarios. We summarize what is known about nitrogen cycling in corals and conclude that disturbance of microbial nitrogen cycling may be tightly linked to coral bleaching and disease.
Relative Diazotroph Abundance in Symbiotic Red Sea Corals Decreases With Water Depth
Microbial dinitrogen (N2) fixation (diazotrophy) is a trait critical for coral holobiont functioning. The contribution of N2 fixation to holobiont nitrogen (N) supply likely depends on the ecological niche of the coral holobiont. Consequently, coral-associated diazotroph communities may exhibit distinct activity patterns across a water depth gradient. We thus compared relative abundances of diazotrophs in the tissues of two common hard coral species, Podabacia sp. and Pachyseris speciosa, along their water depth distribution (10–30 m and 30–50 m, respectively) in the Central Red Sea. The relative gene copy numbers of the nifH gene (i.e., referenced against the eubacterial 16S rRNA gene), as a proxy for N2 fixation potential, were assessed via quantitative PCR. We hypothesized that relative nifH gene copy numbers would decrease with water depth, assuming a related shift from autotrophy to heterotrophy. Findings confirmed this hypothesis and revealed that nifH gene abundances for both corals decreased by ∼97% and ∼90% from the shallowest to the deepest collection site. However, this result was not significant for Pachyseris speciosa due to high biological variability. The observed decrease in nifH gene abundances may be explained by the relative increase in heterotrophy of the coral animal at increasing water depths. Our results underline the importance of interpreting microbial functions and associated nutrient cycling processes within the holobiont in relation to water depth range reflecting steep environmental gradients.
Excess labile carbon promotes the expression of virulence factors in coral reef bacterioplankton
Coastal pollution and algal cover are increasing on many coral reefs, resulting in higher dissolved organic carbon (DOC) concentrations. High DOC concentrations strongly affect microbial activity in reef waters and select for copiotrophic, often potentially virulent microbial populations. High DOC concentrations on coral reefs are also hypothesized to be a determinant for switching microbial lifestyles from commensal to pathogenic, thereby contributing to coral reef degradation, but evidence is missing. In this study, we conducted ex situ incubations to assess gene expression of planktonic microbial populations under elevated concentrations of naturally abundant monosaccharides (glucose, galactose, mannose, and xylose) in algal exudates and sewage inflows. We assembled 27 near-complete (>70%) microbial genomes through metagenomic sequencing and determined associated expression patterns through metatranscriptomic sequencing. Differential gene expression analysis revealed a shift in the central carbohydrate metabolism and the induction of metalloproteases, siderophores, and toxins in Alteromonas, Erythrobacter, Oceanicola, and Alcanivorax populations. Sugar-specific induction of virulence factors suggests a mechanistic link for the switch from a commensal to a pathogenic lifestyle, particularly relevant during increased algal cover and human-derived pollution on coral reefs. Although an explicit test remains to be performed, our data support the hypothesis that increased availability of specific sugars changes net microbial community activity in ways that increase the emergence and abundance of opportunistic pathogens, potentially contributing to coral reef degradation.
Sugar enrichment provides evidence for a role of nitrogen fixation in coral bleaching
The disruption of the coral-algae symbiosis (coral bleaching) due to rising sea surface temperatures has become an unprecedented global threat to coral reefs. Despite decades of research, our ability to manage mass bleaching events remains hampered by an incomplete mechanistic understanding of the processes involved. In this study, we induced a coral bleaching phenotype in the absence of heat and light stress by adding sugars. The sugar addition resulted in coral symbiotic breakdown accompanied by a fourfold increase of coral-associated microbial nitrogen fixation. Concomitantly, increased N:P ratios by the coral host and algal symbionts suggest excess availability of nitrogen and a disruption of the nitrogen limitation within the coral holobiont. As nitrogen fixation is similarly stimulated in ocean warming scenarios, here we propose a refined coral bleaching model integrating the cascading effects of stimulated microbial nitrogen fixation. This model highlights the putative role of nitrogen-fixing microbes in coral holobiont functioning and breakdown.
Ecophysiology of Reef-Building Corals in the Red Sea
The Red Sea is one of the warmest and most saline seas on the planet. Yet, scleractinian corals have managed to flourish under these distinct conditions supporting one of the largest networks of coral reef ecosystems worldwide. Here, we summarize current knowledge on the ecophysiology of reef-building corals gained from 60 years of research in the Red Sea starting from insights in the 1960s to the most recent studies of the past few years. We provide a brief overview over seasonal dynamics and environmental gradients in the Red Sea that are used to study ecophysiological processes of corals under changing environmental and extreme conditions (i.e., temperature, salinity, nutrient, and light availability). We then focus on how this environmental variability shapes the central processes of coral physiology in the Red Sea covering the topics of photosynthesis, calcification, nutrient cycling, and reproduction. We continue by reporting the first physiological measurements of Red Sea deep-sea corals. Last, we discuss how, through the integration of traditional methods with recent developments in the omics field and model systems, we are now beginning to understand the complexity of processes that contribute to the ecological success of corals under these variable conditions. This synthesis may serve as a basis for future studies that aim to contribute to a better understanding of the impacts of environmental change on coral reefs in the Red Sea and the rest of the world.
Dominance of Endozoicomonas bacteria throughout coral bleaching and mortality suggests structural inflexibility of the Pocillopora verrucosa microbiome
The importance of Symbiodinium algal endosymbionts and a diverse suite of bacteria for coral holobiont health and functioning are widely acknowledged. Yet, we know surprisingly little about microbial community dynamics and the stability of host-microbe associations under adverse environmental conditions. To gain insight into the stability of coral host-microbe associations and holobiont structure, we assessed changes in the community structure of Symbiodinium and bacteria associated with the coral Pocillopora verrucosa under excess organic nutrient conditions. Pocillopora-associated microbial communities were monitored over 14 days in two independent experiments. We assessed the effect of excess dissolved organic nitrogen (DON) and excess dissolved organic carbon (DOC). Exposure to excess nutrients rapidly affected coral health, resulting in two distinct stress phenotypes: coral bleaching under excess DOC and severe tissue sloughing (>90% tissue loss resulting in host mortality) under excess DON. These phenotypes were accompanied by structural changes in the Symbiodinium community. In contrast, the associated bacterial community remained remarkably stable and was dominated by two Endozoicomonas phylotypes, comprising on average 90% of 16S rRNA gene sequences. This dominance of Endozoicomonas even under conditions of coral bleaching and mortality suggests the bacterial community of P. verrucosa may be rather inflexible and thereby unable to respond or acclimatize to rapid changes in the environment, contrary to what was previously observed in other corals. In this light, our results suggest that coral holobionts might occupy structural landscapes ranging from a highly flexible to a rather inflexible composition with consequences for their ability to respond to environmental change.
Nitrogen Fixation Aligns with nifH Abundance and Expression in Two Coral Trophic Functional Groups
Microbial nitrogen fixation (diazotrophy) is a functional trait widely associated with tropical reef-building (scleractinian) corals. While the integral role of nitrogen fixation in coral nutrient dynamics is recognized, its ecological significance across different coral functional groups remains yet to be evaluated. Here we set out to compare molecular and physiological patterns of diazotrophy (i.e., nifH gene abundance and expression as well as nitrogen fixation rates) in two coral families with contrasting trophic strategies: highly heterotrophic, free-living members of the family Fungiidae (Pleuractis granulosa, Ctenactis echinata), and mostly autotrophic coral holobionts with low heterotrophic capacity (Pocilloporidae: Pocillopora verrucosa, Stylophora pistillata). The Fungiidae exhibited low diazotroph abundance (based on nifH gene copy numbers) and activity (based on nifH gene expression and the absence of detectable nitrogen fixation rates). In contrast, the mostly autotrophic Pocilloporidae exhibited nifH gene copy numbers and gene expression two orders of magnitude higher than in the Fungiidae, which coincided with detectable nitrogen fixation activity. Based on these data, we suggest that nitrogen fixation compensates for the low heterotrophic nitrogen uptake in autotrophic corals. Consequently, the ecological importance of diazotrophy in coral holobionts may be determined by the trophic functional group of the host.