Corals and their endosymbiotic dinoflagellates of the genus Symbiodinium have a fragile relationship that breaks down under heat stress, an event known as bleaching. However, many coral species have ...adapted to high temperature environments such as the Red Sea (RS). To investigate mechanisms underlying temperature adaptation in zooxanthellate cnidarians we compared transcriptome- and proteome-wide heat stress response (24 h at 32°C) of three strains of the model organism Aiptasia pallida from regions with differing temperature profiles; North Carolina (CC7), Hawaii (H2) and the RS. Correlations between transcript and protein levels were generally low but inter-strain comparisons highlighted a common core cnidarian response to heat stress, including protein folding and oxidative stress pathways. RS anemones showed the strongest increase in antioxidant gene expression and exhibited significantly lower reactive oxygen species (ROS) levels in hospite. However, comparisons of antioxidant gene and protein expression between strains did not show strong differences, indicating similar antioxidant capacity across the strains. Subsequent analysis of ROS production in isolated symbionts confirmed that the observed differences of ROS levels in hospite were symbiont-driven. Our findings indicate that RS anemones do not show increased antioxidant capacity but may have adapted to higher temperatures through association with more thermally tolerant symbionts.
High internal phase Pickering emulsions (HIPPEs) stabilized by food-grade proteins have attracted much attention. In this study, Spanish mackerel protein (SMP)-procyanidin (PC) hybrid nanoparticles ...(SPHPs) were prepared through electrostatic interactions and hydrogen bonding as an emulsifier for HIPPEs. Transmission electron microscopy (TEM) showed that, unlike the spherical SMPs, the SPHPs had a cross-linked structure with rough surface. The particle size of HIPPE droplets decreased with increasing SPHP concentration. Photographs and magnetic resonance imaging (MRI) showed that the HIPPEs stabilized by SPHPs had a stable gel structure and the oil protons were evenly distributed when the oil fraction of HIPPEs was 85%. Low-field nuclear magnetic resonance (LF-NMR) transverse relaxation showed that the water state in HIPPEs stabilized by SPHPs was mainly immobilized and showed good stability after 4 weeks of storage. Rheological analysis showed that the HIPPEs had good viscoelasticity and thixotropy. Simulated digestion experiments showed that the HIPPEs improved the bioaccessibility of astaxanthin. The application of HIPPEs in surimi products shows that HIPPEs in surimi had a high adhesion rate (47.89%) and good cooking stability. HIPPEs stabilized by SPHPs could achieve efficient delivery of astaxanthin and had the potential to be applied to functional surimi products in the form of simple adhesion.
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•Spanish mackerel protein-procyanidin particles were prepared to stabilize HIPPEs.•Procyanidins boosted the emulsifying capacity of Spanish mackerel proteins.•HIPPEs have solid-like gel properties and long-term stability.•HIPPEs improved the stability and bioaccessibility of astaxanthin.•HIPPEs applied to surimi had high adhesion and good cooking stability.
The metabolic symbiosis with photosynthetic algae allows corals to thrive in the oligotrophic environments of tropical seas. Different aspects of this relationship have been investigated using the ...emerging model organism Aiptasia. However, many fundamental questions, such as the nature of the symbiotic relationship and the interactions of nutrients between the partners remain highly debated. Using a meta-analysis approach, we identified a core set of 731 high-confidence symbiosis-associated genes that revealed host-dependent recycling of waste ammonium and amino acid synthesis as central processes in this relationship. Subsequent validation via metabolomic analyses confirmed that symbiont-derived carbon enables host recycling of ammonium into nonessential amino acids. We propose that this provides a regulatory mechanism to control symbiont growth through a carbon-dependent negative feedback of nitrogen availability to the symbiont. The dependence of this mechanism on symbiont-derived carbon highlights the susceptibility of this symbiosis to changes in carbon translocation, as imposed by environmental stress.
In hermatypic scleractinian corals, photosynthetic fixation of CO2 and the production of CaCO3 are intimately linked due to their symbiotic relationship with dinoflagellates of the Symbiodiniaceae ...family. This makes it difficult to study ion transport mechanisms involved in the different pathways. In contrast, most ahermatypic scleractinian corals do not share this symbiotic relationship and thus offer an advantage when studying the ion transport mechanisms involved in the calcification process. Despite this advantage, non-symbiotic scleractinian corals have been systematically neglected in calcification studies, resulting in a lack of data especially at the molecular level. Here, we combined a tissue micro-dissection technique and RNA-sequencing to identify calcification-related ion transporters, and other candidates, in the ahermatypic non-symbiotic scleractinian coral Tubastraea spp. Our results show that Tubastraea spp. possesses several calcification-related candidates previously identified in symbiotic scleractinian corals (such as SLC4-γ, AMT-1like, CARP, etc.). Furthermore, we identify and describe a role in scleractinian calcification for several ion transporter candidates (such as SLC13, -16, -23, etc.) identified for the first time in this study. Taken together, our results provide not only insights about the molecular mechanisms underlying non-symbiotic scleractinian calcification, but also valuable tools for the development of biotechnological solutions to better control the extreme invasiveness of corals belonging to this particular genus.
Abstract
Symbiotic associations with Symbiodiniaceae have evolved independently across a diverse range of cnidarian taxa including reef-building corals, sea anemones, and jellyfish, yet the molecular ...mechanisms underlying their regulation and repeated evolution are still elusive. Here, we show that despite their independent evolution, cnidarian hosts use the same carbon-nitrogen negative feedback loop to control symbiont proliferation. Symbiont-derived photosynthates are used to assimilate nitrogenous waste via glutamine synthetase–glutamate synthase-mediated amino acid biosynthesis in a carbon-dependent manner, which regulates the availability of nitrogen to the symbionts. Using nutrient supplementation experiments, we show that the provision of additional carbohydrates significantly reduces symbiont density while ammonium promotes symbiont proliferation. High-resolution metabolic analysis confirmed that all hosts co-incorporated glucose-derived
13
C and ammonium-derived
15
N via glutamine synthetase–glutamate synthase-mediated amino acid biosynthesis. Our results reveal a general carbon-nitrogen negative feedback loop underlying these symbioses and provide a parsimonious explanation for their repeated evolution.
The symbiotic relationship between cnidarians and dinoflagellates is one of the most widespread endosymbiosis in our oceans and provides the ecological basis of coral reef ecosystems. Although many ...studies have been undertaken to unravel the molecular mechanisms underlying these symbioses, we still know little about the epigenetic mechanisms that control the transcriptional responses to symbiosis. Here, we used the model organism Exaiptasia diaphana to study the genome-wide patterns and putative functions of the histone modifications H3K27ac, H3K4me3, H3K9ac, H3K36me3, and H3K27me3 in symbiosis. While we find that their functions are generally conserved, we observed that colocalization of more than one modification and or DNA methylation correlated with significantly higher gene expression, suggesting a cooperative action of histone modifications and DNA methylation in promoting gene expression. Analysis of symbiosis genes revealed that activating histone modifications predominantly associated with symbiosis-induced genes involved in glucose metabolism, nitrogen transport, amino acid biosynthesis, and organism growth while symbiosis-suppressed genes were involved in catabolic processes. Our results provide new insights into the mechanisms of prominent histone modifications and their interaction with DNA methylation in regulating symbiosis in cnidarians.
Modern transformation and genome editing techniques have shown great success across a broad variety of organisms. However, no study of successfully applied genome editing has been reported in a ...dinoflagellate despite the first genetic transformation of Symbiodinium being published about 20 years ago. Using an array of different available transformation techniques, we attempted to transform Symbiodinium microadriaticum (CCMP2467), a dinoflagellate symbiont of reef-building corals, with the view to performing subsequent CRISPR-Cas9 mediated genome editing. Plasmid vectors designed for nuclear transformation containing the chloramphenicol resistance gene under the control of the CaMV p35S promoter as well as several putative endogenous promoters were used to test a variety of transformation techniques including biolistics, electroporation and agitation with silicon carbide whiskers. Chloroplast-targeted transformation was attempted using an engineered Symbiodinium chloroplast minicircle encoding a modified PsbA protein expected to confer atrazine resistance. We report that we have been unable to confer chloramphenicol or atrazine resistance on Symbiodinium microadriaticum strain CCMP2467.
The coral-Symbiodiniaceae symbiosis is fundamental for the coral reef ecosystem. Corals provide various inorganic nutrients to their algal symbionts in exchange for the photosynthates to meet their ...metabolic demands. When becoming symbionts, Symbiodiniaceae cells show a reduced proliferation rate and a different life history. While it is generally believed that the animal hosts play critical roles in regulating these processes, far less is known about the molecular underpinnings that allow the corals to induce the changes in their symbionts.
We tested symbiont cell proliferation and life stage changes in vitro in response to different nutrient-limiting conditions to determine the key nutrients and to compare the respective symbiont transcriptomic profiles to cells in hospite. We then examined the effects of nutrient repletion on symbiont proliferation in coral hosts and quantified life stage transitions in vitro using time-lapse confocal imaging. Here, we show that symbionts in hospite share gene expression and pathway activation profiles with free-living cells under nitrogen-limited conditions, strongly suggesting that symbiont proliferation in symbiosis is limited by nitrogen availability.
We demonstrate that nitrogen limitation not only suppresses cell proliferation but also life stage transition to maintain symbionts in the immobile coccoid stage. Nutrient repletion experiments in corals further confirmed that nitrogen availability is the major factor limiting symbiont density in hospite. Our study emphasizes the importance of nitrogen in coral-algae interactions and, more importantly, sheds light on the crucial role of nitrogen in symbiont life history regulation.
The symbiotic relationship between cnidarians and dinoflagellates is the cornerstone of coral reef ecosystems. Although research has focused on the molecular mechanisms underlying this symbiosis, the ...role of epigenetic mechanisms, that is, the study of heritable changes that do not involve changes in the DNA sequence, is unknown. To assess the role of DNA methylation in the cnidarian-dinoflagellate symbiosis, we analyzed genome-wide CpG methylation, histone associations, and transcriptomic states of symbiotic and aposymbiotic anemones in the model system Aiptasia. We found that methylated genes are marked by histone 3 lysine 36 trimethylation (H3K36me3) and show significant reduction of spurious transcription and transcriptional noise, revealing a role of DNA methylation in the maintenance of transcriptional homeostasis. Changes in DNA methylation and expression show enrichment for symbiosis-related processes, such as immunity, apoptosis, phagocytosis recognition, and phagosome formation, and reveal intricate interactions between the underlying pathways. Our results demonstrate that DNA methylation provides an epigenetic mechanism of transcriptional homeostasis that responds to symbiosis.
Rising sea surface temperature is the main cause of global coral reef decline. Abnormally high temperatures trigger the breakdown of the symbiotic association between corals and their photosynthetic ...symbionts in the genus Symbiodinium. Higher genetic variation resulting from shorter generation times has previously been proposed to provide increased adaptability to Symbiodinium compared to the host. Retrotransposition is a significant source of genetic variation in eukaryotes and some transposable elements are specifically expressed under adverse environmental conditions. We present transcriptomic and phylogenetic evidence for the existence of heat stress-activated Ty1-copia-type LTR retrotransposons in the coral symbiont Symbiodinium microadriaticum. Genome-wide analyses of emergence patterns of these elements further indicate recent expansion events in the genome of S. microadriaticum. Our findings suggest that acute temperature increases can activate specific retrotransposons in the Symbiodinium genome with potential impacts on the rate of retrotransposition and the generation of genetic variation under heat stress.
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