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Background The stability of the symbiotic relationship between coral and their dinoflagellate algae (Symbiodiniaceae) is disrupted by ocean warming. Although the coral thermal response depends on the complex interactions between host, Symbiodiniaceae and prokaryotes, the mechanisms underlying the initial destabilization of these symbioses are poorly understood. Results In a 2-month manipulative experiment, we exposed the coral Porites lutea to gradually increasing temperatures corresponding to 0–8 degree heating weeks (DHW) and assessed the response of the coral holobiont using coral and Symbiodiniaceae transcriptomics, microbial 16S rRNA gene sequencing and physiological measurements. From early stages of heat stress (< 1 DHW), the increase in metabolic turnover shifted the holobiont to a net heterotrophic state in which algal-derived nutrients were insufficient to meet host energy demands, resulting in reduced holobiont performance at 1 DHW. We postulate the altered nutrient cycling also affected the coral-associated microbial community, with the relative abundance of Endozoicomonas bacteria declining under increasing heat stress. Integration of holobiont stress responses correlated this decline to an increase in expression of a host ADP-ribosylation factor, suggesting that Symbiodiniaceae and Endozoicomonas may underlie similar endosymbiotic regulatory processes. Conclusions The thermotolerance of coral holobionts therefore is influenced by the nutritional status of its members and their interactions, and this identified metabolic interdependency highlights the importance of applying an integrative approach to guide coral reef conservation efforts. 1eX9fiMXdD4vUDcCw31JRU Video Abstract

Disease is an increasing threat to reef-building corals. One of the few identified pathogens of coral disease is the bacterium Vibrio coralliilyticus . In Vibrio cholerae , infection by a bacterial virus (bacteriophage) results in the conversion of non-pathogenic strains to pathogenic strains and this can lead to cholera pandemics. Pathogenicity islands encoded in the V. cholerae genome play an important role in pathogenesis. Here we analyse five whole genome sequences of V. coralliilyticus to examine whether virulence is similarly driven by horizontally acquired elements. We demonstrate that bacteriophage genomes encoding toxin genes with homology to those found in pathogenic V. cholerae are integrated in V. coralliilyticus genomes. Virulence factors located on chromosomal pathogenicity islands also exist in some strains of V. coralliilyticus . The presence of these genetic signatures indicates virulence in V. coralliilyticus is driven by prophages and other horizontally acquired elements. Screening for pathogens of coral disease should target conserved regions in these elements.

Despite the relevance of heat‐evolved microalgal endosymbionts to coral reef restoration, to date, few Symbiodiniaceae strains have been thermally enhanced via experimental evolution. Here, we investigated whether the thermal tolerance of Symbiodiniaceae can be increased through chemical mutagenesis followed by thermal selection. Strains of Durusdinium trenchii, Fugacium kawagutii and Symbiodinium pilosum were exposed to ethyl methanesulfonate to induce random mutagenesis, and then underwent thermal selection at high temperature (31/33°C). After 4.6–5 years of experimental evolution, the in vitro thermal tolerance of these strains was assessed via reciprocal transplant experiments to ambient (27°C) and elevated (31/35°C) temperatures. Growth, photosynthetic efficiency, oxidative stress and nutrient use were measured to compare thermal tolerance between strains. Heat‐evolved D. trenchii, F. kawagutii and S. pilosum strains all exhibited increased photosynthetic efficiency under thermal stress. However, trade‐offs in growth rates were observed for the heat‐evolved D. trenchii lineage at both ambient and elevated temperatures. Reduced phosphate and nitrate uptake rates in F. kawagutii and S. pilosum heat‐evolved lineages, respectively, suggest alterations in nutrition resource usage and allocation processes may have occurred. Increased phosphate uptake rates of the heat‐evolved D. trenchii strain indicate that experimental evolution resulted in further trade‐offs in this species. These findings deepen our understanding of the physiological responses of Symbiodiniaceae cultures to thermal selection and their capacity to adapt to elevated temperatures. The new heat‐evolved Symbiodiniaceae developed here may be beneficial for coral reef restoration efforts if their enhanced thermal tolerance can be conferred in hospite.

Here we describe an efficient and effective technique for rearing sexually-derived coral propagules from spawning through larval settlement and symbiont uptake with minimal impact on natural coral populations. We sought to maximize larval survival while minimizing expense and daily husbandry maintenance by experimentally determining optimized conditions and protocols for gamete fertilization, larval cultivation, induction of larval settlement by crustose coralline algae, and inoculation of newly settled juveniles with their dinoflagellate symbiont Symbiodinium . Larval rearing densities at or below 0.2 larvae mL −1 were found to maximize larval survival and settlement success in culture tanks while minimizing maintenance effort. Induction of larval settlement via the addition of a ground mixture of diverse crustose coralline algae (CCA) is recommended, given the challenging nature of in situ CCA identification and our finding that non settlement-inducing CCA assemblages do not inhibit larval settlement if suitable assemblages are present. Although order of magnitude differences in infectivity were found between common Great Barrier Reef Symbiodinium clades C and D, no significant differences in Symbiodinium uptake were observed between laboratory-cultured and wild-harvested symbionts in each case. The technique presented here for Acropora millepora can be adapted for research and restoration efforts in a wide range of broadcast spawning coral species.

Corals’ tolerance to high temperature stress largely depends on their symbiotic microalgae (Symbiodiniaceae). However, the contributing microalgal traits and their relationships to one another are largely unclear. Here we compare the in vitro cellular profiles of seven Cladocopium C1 acro microalgal strains (derived from the same ancestral strain) during a four-week exposure to 27°C or 31°C. One was an unselected wild-type strain (WT), three were selected at 31°C for nine years and shown to confer thermal tolerance on the coral host (SS+) and three others were similarly selected but did not confer tolerance (SS-). Flow cytometry was used to measure the staining intensities of cells treated with dyes representing the intracellular stress indicators reactive oxygen species (ROS), reduced glutathione (rGSH) and mitochondrial activity, as well as cell size/shape and photosynthetic pigments. Cell densities and photosynthetic efficiency (ϕPSII, F v /F m ) were also measured. WT showed the highest levels of intracellular ROS and mitochondrial activity, lowest rGSH and largest cell sizes at both temperatures. SS+ strains had the lowest ROS and highest rGSH values and a unique pattern of correlations among parameters at 31°C. Our results support previous reports implicating the role of microalgal ROS, mitochondria and rGSH in holobiont thermal tolerance and suggest flow cytometry is a useful screening tool for identifying microalgal strains with enhanced thermal tolerance.

Coral cover worldwide has been declining due to heat stress caused by climate change. Here we report the impacts of the 2015–2016 El Niño mass coral bleaching event on the coral cover of reefs located on central and northern atolls of the Maldives. We surveyed six reef sites in the Alifu Alifu (Ari) and Baa (South Maalhosmadulu) Atolls using replicate 20 m benthic photo transects at two depths per reef site. Live and recently dead coral cover identified from images differed between reef sites and depth. Recently dead corals on average made up 33% of the coral assemblage at shallow sites and 24% at deep sites. This mortality was significantly lower in massive corals than in branching corals, reaching an average of only 6% compared to 41%, respectively. The best predictors of live coral cover were depth and morphology, with a greater percentage of live coral at deep sites and in massive corals. The same predictors best described the prevalence of recently dead coral, but showed inverse trends to live coral. However, there was high variability among reef sites, which could be attributed to additional local stressors. Coral bleaching and resulting coral mortalities, such as the ones reported here, are of particular concern for small island nations like the Maldives, which are reliant on coral reefs.

Black band disease (BBD) is a common disease of reef-building corals with a worldwide distribution that causes tissue loss at a rate of up to 3 cm/day. Critical for a mechanistic understanding of the disease’s aetiology is the cultivation of its proposed pathogen, filamentous cyanobacteria (genus Roseofilum ). Here, we optimise existing protocols for the isolation and cultivation of Roseofilum cyanobacteria using a new strain from the central Great Barrier Reef. We demonstrate that the isolation of this bacterium via inoculation onto agar plates was highly effective with a low percentage agar of 0.6% and that growth monitoring was most sensitive with fluorescence measurements of chlorophyll-a (440/685 nm). Cell growth curves in liquid and solid media were generated for the first time for this cyanobacterium and showed best growth rates for the previously untested L1-medium (growth rate k = 0.214 biomass/day; doubling time t gen = 4.67 days). Our results suggest that the trace metals contained in L1-medium maximise biomass increase over time for this cyanobacterium. Since the newly isolated Roseofilum strain is genetically closest to Pseudoscillatoria coralii , but in terms of pigmentation and cell size closer to Roseofilum reptotaenium , we formally merge the two species into a single taxon by providing an emended species description, Roseofilum reptotaenium (Rasoulouniriana) Casamatta emend. Following this optimized protocol is recommended for fast isolation and cultivation of Roseofilum cyanobacteria, for growth curve generation in strain comparisons and for maximisation of biomass in genetic studies.

In this study, a flame-generated nm-range SiO2 aerosol (approx. 170 nm median aggregate diameter) is fed into an electrostatic precipitator with an operating temperature of 200 °C. While a highly porous layer of SiO2 nanoparticles (NPs) is deposited by electrostatic precipitation, a decrease of current uptake is observed initially, indicating exceptionally high values of the electric field within the layer (> 100 kV/mm) and of the layer resistivity (> 1013 Ω∙cm). Later a strong (13- to 17-fold) increase of current uptake is observed. Aerosol charge measurements show that charges of opposite polarity are emitted from the NP layer. Investigation of the NP layer by SEM shows that charge-emitting structures with a polarity-dependent morphology develop on an originally homogeneous NP layer. Based on the experimental evidence, the mechanisms of charge emission and structure formation are discussed. Charge emission from the precipitated dust layer is known as back corona in the field of electrostatic precipitation. It appears that the mechanisms of back corona observed with SiO2 NP layers are quite distinct from those observed with µm-range particles. While gas discharges inside the NP layer are suppressed due to small pore size, back corona inside the NP layers is apparently initiated by thermionic field emission of free electrons and secondary electron multiplication within the NP layer.

Early life stages of most coral species acquire microalgal endosymbionts (Symbiodiniaceae) from the environment, but whether exogenous symbiont uptake is possible in the adult life stage is unclear. Deep sequencing of the Symbiodiniaceae ITS2 genetic marker has revealed novel symbionts in adult corals following bleaching; however these strains may have already been present at densities below detection limits. To test whether acquisition of symbionts from the environment occurs, we subjected adult fragments of corals (six species in four families) to a chemical bleaching treatment (menthol and DCMU). The treatment reduced the native microalgal symbiont abundance to below 2% of their starting densities. The bleached corals were then inoculated with a cultured Cladocopium C1 acro strain. Genotyping of the Symbiodiniaceae communities before bleaching and after reinoculation showed that fragments of all six coral species acquired the Cladocopium C1 acro strain used for inoculation. Our results provide strong evidence for the uptake of Symbiodiniaceae from the environment by adult corals. We also demonstrate the feasibility of chemical bleaching followed by reinoculation to manipulate the Symbiodiniaceae communities of adult corals, providing an innovative approach to establish new symbioses between adult corals and heat-evolved microalgal symbionts, which could prove highly relevant to coral reef restoration efforts.

Heat-tolerant strains of the coral endosymbiont, Cladocopium C1acro (Symbiodiniaceae), have previously been developed via experimental evolution. Here, we examine physiological responses and bacterial community composition (using 16S rRNA gene metabarcoding) in cultures of 10 heat-evolved (SS) and 9 wild-type (WT) strains, which had been exposed for 6 years to 31 °C and 27 °C, respectively. We also examine whether the associated bacterial communities were affected by a three-week reciprocal transplantation to both temperatures. The SS strains had bacterial communities with lower diversities that showed more stability and lower variability when exposed to elevated temperatures compared with the WT strains. Amplicon sequence variants (ASVs) of the bacterial genera Labrenzia, Algiphilus, Hyphobacterium and Roseitalea were significantly more associated with the SS strains compared with the WT strains. WT strains showed higher abundance of ASVs assigned to the genera Fabibacter and Tropicimonas. We hypothesize that these compositional differences in associated bacterial communities between SS and WT strains also contribute to the thermal tolerance of the microalgae. Future research should explore functional potential between bacterial communities using metagenomics to unravel specific genomic adaptations.