Rädecker, Nils
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Presence of algal symbionts affects denitrifying bacterial communities in the sea anemone Aiptasia coral model
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.
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.
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.
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.
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.
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.