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.
Nutrient stress arrests tentacle growth in the coral model Aiptasia
The symbiosis between cnidarians and dinoflagellate algae of the family Symbiodiniaceae builds the foundation of coral reef ecosystems. The sea anemone Aiptasia is an emerging model organism promising to advance our functional understanding of this symbiotic association. Here, we report the observation of a novel phenotype of symbiotic Aiptasia likely induced by severe nutrient starvation. Under these conditions, developing Aiptasia no longer grow any tentacles. At the same time, fully developed Aiptasia do not lose their tentacles, yet produce asexual offspring lacking tentacles. This phenotype, termed ‘Wurst’ Aiptasia, can be easily induced and reverted by nutrient starvation and addition, respectively. Thereby, this observation may offer a new experimental framework to study mechanisms underlying phenotypic plasticity as well as nutrient cycling within the Cnidaria – Symbiodiniaceae symbiosis.
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.
High salinity conveys thermotolerance in the coral model Aiptasia
The endosymbiosis between dinoflagellate algae of the genus Symbiodinium and stony corals provides the foundation of coral reef ecosystems. Coral bleaching, the expulsion of endosymbionts from the coral host tissue as a consequence of heat or light stress, poses a threat to reef ecosystem functioning on a global scale. Hence, a better understanding of the factors contributing to heat stress susceptibility and tolerance is needed. In this regard, some of the most thermotolerant corals live in particularly saline habitats, but possible effects of high salinity on thermotolerance in corals are anecdotal. Here we test the hypothesis that high salinity may lead to increased thermotolerance. We conducted a heat stress experiment at low, intermediate, and high salinities using a set of host-endosymbiont combinations of the coral model Aiptasia. As expected, all host-endosymbiont combinations showed reduced photosynthetic efficiency and endosymbiont loss during heat stress, but the severity of bleaching was significantly reduced with increasing salinities for one of the host-endosymbiont combinations. Our results show that higher salinities can convey increased thermotolerance in Aiptasia, although this effect seems to be dependent on the particular host strain and/or associated symbiont type. This finding may help explain the extraordinarily high thermotolerance of corals in high salinity environments, such as the Red Sea and the Persian/Arabian Gulf, and provides novel insight regarding factors that contribute to thermotolerance. Since our results are based on a salinity effect in symbiotic sea anemones, it remains to be determined whether this salinity effect can also be observed in stony corals.
High levels of floridoside at high salinity link osmoadaptation with bleaching susceptibility in the cnidarian-algal endosymbiosis
Coral reefs are in global decline mainly due to increasing sea surface temperatures triggering coral bleaching. Recently, high salinity has been linked to increased thermotolerance and decreased bleaching in the sea anemone coral model Aiptasia. However, the underlying processes remain elusive. Using two Aiptasia host–endosymbiont pairings, we induced bleaching at different salinities and show reduced reactive oxygen species (ROS) release at high salinities, suggesting a role of osmoadaptation in increased thermotolerance. A subsequent screening of osmolytes revealed that this effect was only observed in algal endosymbionts that produce 2-O-glycerol-α-D-galactopyranoside (floridoside), an osmolyte capable of scavenging ROS. This result argues for a mechanistic link between osmoadaptation and thermotolerance, mediated by ROS-scavenging osmolytes (e.g., floridoside). This sheds new light on the putative mechanisms underlying the remarkable thermotolerance of corals from water bodies with high salinity such as the Red Sea or Persian/Arabian Gulf and holds implications for coral thermotolerance under climate change.
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.
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.
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.
Metaorganisms in extreme environments : do microbes play a role in organismal adaptation?
From protists to humans, all animals and plants are inhabited by microbial organisms. There is an increasing appreciation that these resident microbes influence the fitness of their plant and animal hosts, ultimately forming a metaorganism consisting of a uni- or multicellular host and a community of associated microorganisms. Research on host-microbe interactions has become an emerging cross-disciplinary field. In both vertebrates and invertebrates a complex microbiome confers immunological, metabolic and behavioural benefits; conversely, its disturbance can contribute to the development of disease states. However, the molecular and cellular mechanisms controlling the interactions within a metaorganism are poorly understood and many key interactions between the associated organisms remain unknown. In this perspective article, we outline some of the issues in interspecies interactions and in particular address the question of how metaorganisms react and adapt to inputs from extreme environments such as deserts, the intertidal zone, oligothrophic seas, and hydrothermal vents.
Using Aiptasia as a Model to Study Metabolic Interactions in Cnidarian-Symbiodinium Symbioses
The symbiosis between cnidarian hosts and microalgae of the genus Symbiodinium provides the foundation of coral reefs in oligotrophic waters. Understanding the nutrient-exchange between these partners is key to identifying the fundamental mechanisms behind this symbiosis, yet has proven difficult given the endosymbiotic nature of this relationship. In this study, we investigated the respective contribution of host and symbiont to carbon and nitrogen assimilation in the coral model anemone Aiptaisa. For this, we combined traditional measurements with nanoscale secondary ion mass spectrometry (NanoSIMS) and stable isotope labeling to investigate patterns of nutrient uptake and translocation both at the organismal scale and at the cellular scale. Our results show that the rate of carbon and nitrogen assimilation in Aiptasia depends on the identity of the host and the symbiont. NanoSIMS analysis confirmed that both host and symbiont incorporated carbon and nitrogen into their cells, implying a rapid uptake and cycling of nutrients in this symbiotic relationship. Gross carbon fixation was highest in Aiptasia associated with their native Symbiodinium communities. However, differences in fixation rates were only reflected in the δ13C enrichment of the cnidarian host, whereas the algal symbiont showed stable enrichment levels regardless of host identity. Thereby, our results point toward a "selfish" character of the cnidarian-Symbiodinium association in which both partners directly compete for available resources. Consequently, this symbiosis may be inherently instable and highly susceptible to environmental change. While questions remain regarding the underlying cellular controls of nutrient exchange and the nature of metabolites involved, the approach outlined in this study constitutes a powerful toolset to address these questions.