Population dynamics of dominant dinoflagellate species in the North Sea: in situ growth rates, photosynthetic potential, and losses due to parasitism.

In the North Sea, Tripos and Dinophysis are commonly occurring mixotrophic planktonic dinoflagellate genera. In order to understand their bloom dynamics, an occurring bloom dominated by T. furca and D. norvegica was followed for several days. High cell abundances of these species were located to estimate: in situ growth rates from cell cycle analyses, depth distributions, growth rates sustained by photosynthesis, and parasite infection prevalence in all T. furca, T. fusus, D. norvegica and D. acuminata. Cell abundances were over 10000 cells L-1 for T. furca and up to 18000 cells L-1 for D. norvegica. Cells accumulated between 15-25 m depth and presented low specific in situ growth rates of 0.04-0.15 d-1 for T. furca and 0.02-0.16 d-1 for D. norvegica. Photosynthesis could sustain growth rates of 0.01-0.18 d-1 for T. furca and 0.02 to 0.14 d-1 for D. norvegica, suggesting that these species were relying mainly on photosynthesis. Parasite infections where generally low, with occasional high prevalence in D. norvegica (by Parvilucifera sp.) and T. fusus (by Amoebophrya sp.), while both parasites showed comparable prevalence in D. acuminata, which could offset in situ growth rates by parasite-induced host mortality. The restructuring effect of parasites on dinoflagellate blooms is often overlooked and this study elucidates their effect to cell abundances and their growth at the final stages of a bloom.

Succession of diversity, assembly mechanisms, and activities of the microeukaryotic community throughout Scrippsiella acuminata (Dinophyceae) bloom phases.

Harmful algal bloom (HAB) is a rapidly expanding marine ecological hazard. Although numerous studies have been carried out about the ecological impact and the ecological mechanism of HAB outbreaks, few studies have comprehensively addressed the shifts of species composition, metabolic activity level, driving factors and community assembly mechanisms of microeukaryotic plankton in the course of the bloom event. To fill the gap of research, we conducted 18S ribosomal DNA and RNA sequencing during the initiation, development, sustenance and decline stages of a Scrippsiella acuminata (S. acuminata) bloom at the coastal sea of Fujian Province, China. We found that the bloom event caused a decrease in microeukaryotic plankton species diversity and increase in community homogeneity. Our results revealed that the RNA- and DNA-inferred communities were similar, but α-diversity was more dynamic in RNA- than in DNA-inferred communities. The main taxa with high projected metabolic activity (with RNA:DNA ratio as the proxy) during the bloom included dinoflagellates, Cercozoa, Chlorophyta, Protalveolata, and diatoms. The role of deterministic processes in microeukaryotic plankton community assembly increased during the bloom, but stochastic processes were always the dominant assembly mechanism throughout the bloom process. Our findings improve the understanding of temporal patterns, driving factors and assembly mechanisms underlying the microeukarytic plankton community in a dinoflagellate bloom.

Mesocosm study of PAC-modified clay effects on Karenia brevis cells and toxins, chemical dynamics, and benthic invertebrate physiology.

Modified clay compounds are used globally as a method of controlling harmful algal blooms, and their use is currently under consideration to control Karenia brevis blooms in Florida, USA. In 1400 L mesocosm tanks, chemical dynamics and lethal and sublethal impacts of MC II, a polyaluminum chloride (PAC)-modified kaolinite clay, were evaluated over 72 h on a benthic community representative of Sarasota Bay, which included blue crab (Callinectes sapidus), sea urchin (Lytechinus variegatus), and hard clam (Mercenaria campechiensis). In this experiment, MC II was dosed at 0.2 g L-1 to treat bloom-level densities of K. brevis at 1 × 106 cells L-1. Cell removal in MC II-treated tanks was 57% after 8 h and 95% after 48 h. In the water column, brevetoxin analogs BTx-1 and BTx-2 were found to be significantly higher in untreated tanks at 24 and 48 h, while in MC II-treated tanks, BTx-3 was found to be higher at 48 h and BTx-B5 was found to be higher at 24 and 48 h. In MC II floc, we found no significant differences in BTx-1 or BTx-2 between treatments for any time point, while BTx-3 was found to be significantly higher in the MC II-treated tanks at 48 and 72 h, and BTx-B5 was higher in MC II-treated tanks at 24 and 72 h. Among various chemical dynamics observed, it was notable that dissolved phosphorus was consistently significantly lower in MC II tanks after 2 h, and that turbidity in MC II tanks returned to control levels 48 h after treatment. Dissolved inorganic carbon and total seawater alkalinity were significantly reduced in MC II tanks, and partial pressure of CO2 (pCO2) was significantly higher in the MC II-only treatment after 2 h. In MC II floc, particulate phosphorus was found to be significantly higher in MC II tanks after 24 h. In animals, lethal and sublethal responses to MC II-treated K. brevis did not differ from untreated K. brevis for either of our three species at any time point, suggesting MC II treatment at this dosage has negligible impacts to these species within 72 h of exposure. These results appear promising in terms of the environmental safety of MC II as a potential bloom control option, and we recommend scaling up MC II experiments to field trials in order to gain deeper understanding of MC II performance and dynamics in natural waters.

Antagonistic interactions of the dinoflagellate Alexandrium catenella under simultaneous warming and acidification.

There is a concern that harmful algal bloom (HAB) species may increase under climate change. Yet, we lack understanding of how ecological interactions will be affected under ocean warming and acidification (OWA) conditions. We tested the antagonistic effects of three strains of the dinoflagellate HAB species Alexandrium catenella on three target species (the chlorophyte Tetraselmis sp., the cryptomonad Rhodomonas salina, and the diatom Thalassiosira weissflogii) at various biomass ratios between species, at ambient (16 °C and 400 µatm CO2) and OWA (20 °C and 2000 µatm CO2) conditions. In these experiments the Alexandrium strains had been raised under OWA conditions for ∼100 generations. All three non-HAB species increased their growth rate under OWA relative to ambient conditions. Growth rate inhibition was evident for R. salina and Tetraselmis sp. under OWA conditions, but not under ambient conditions. These negative effects were exacerbated at higher concentrations of Alexandrium relative to non-HAB species. By contrast, T. weissflogii showed positive growth in the presence of two strains of Alexandrium under ambient conditions, whereas growth was unaffected under OWA. Contrary to our expectations, A. catenella had a slight negative response in the presence of the diatom. These results demonstrate that Alexandrium exerts higher antagonistic effects under OWA compared to ambient conditions, and these effects are species-specific and density dependent. These negative effects may shift phytoplankton community composition under OWA conditions.

Allelochemicals of Alexandrium tamarense and its algicidal mechanism for Prorocentrum donghaiense and Heterosigma akashiwo.

The effects of culture filtrate of Alexandrium tamarense on Prorocentrum donghaiense and Heterosigma akashiwo were investigated, including determination of algal density, photosynthesis, intracellular enzyme content and activity. The filtrate of A. tamarense had a stronger inhibitory effect on P. donghaiense than H. akashiwo, and the inhibitory effect decreased with higher temperature treatment of the filtrate. Instantaneous fluorescence (Ft) and maximum quantum yield of photosystem II (Fv/Fm) values of both kinds of target algae were reduced as exposed to the filtrate of A. tamarense, which proved that allelopathy could inhibit the normal operation of photosynthetic system. The increase of Malondialdehyde (MDA) content of the two kinds of target algae indicated that the cell membrane was seriously damaged by allelochemicals released by A. tamarense. The different responses of Superoxide Dismutase (SOD) and Catalase (CAT) activity in two kinds of target algae demonstrated the complexity and diversity of allelopathic mechanism. The filtrate of A. tamarense also influenced the metabolic function (ATPases) of P. donghaiense and H. akashiwo, and the influence on P. donghaiense was greater. Liquid-liquid extraction was used to extract and isolate allelochemicals from the filtrate of A. tamarense. It was found that only component I with molecular weight of 424.2573 and 434.2857 could inhibit the growth of P. donghaiense by HPLC-MS.

Coral-infecting parasites in cold marine ecosystems.

Coral reefs are a biodiversity hotspot,1,2 and the association between coral and intracellular dinoflagellates is a model for endosymbiosis.3,4 Recently, corals and related anthozoans have also been found to harbor another kind of endosymbiont, apicomplexans called corallicolids.5 Apicomplexans are a diverse lineage of obligate intracellular parasites6 that include human pathogens such as the malaria parasite, Plasmodium.7 Global environmental sequencing shows corallicolids are tightly associated with tropical and subtropical reef environments,5,8,9 where they infect diverse corals across a range of depths in many reef systems, and correlate with host mortality during bleaching events.10 All of this points to corallicolids being ecologically significant to coral reefs, but it is also possible they are even more widely distributed because most environmental sampling is biased against parasites that maintain a tight association with their hosts throughout their life cycle. We tested the global distribution of corallicolids using a more direct approach, by specifically targeting potential anthozoan host animals from cold/temperate marine waters outside the coral reef context. We found that corallicolids are in fact common in such hosts, in some cases at high frequency, and that they infect the same tissue as parasites from topical coral reefs. Parasite phylogeny suggests corallicolids move between hosts and habitats relatively frequently, but that biogeography is more conserved. Overall, these results greatly expand the range of corallicolids beyond coral reefs, suggesting they are globally distributed parasites of marine anthozoans, which also illustrates significant blind spots that result from strategies commonly used to sample microbial biodiversity.

Nutrient depletion and heat stress impair the assimilation of nitrogen compounds in a scleractinian coral.

Concentrations of dissolved nitrogen in seawater can affect the resilience of the cnidarian-dinoflagellate symbiosis to climate change-induced bleaching. However, it is not yet known how the assimilation and translocation of the various nitrogen forms change during heat stress, nor how the symbiosis responds to nutrient depletion, which may occur due to increasing water stratification. Here, the tropical scleractinian coral Stylophora pistillata, in symbiosis with dinoflagellates of the genus Symbiodinium, was grown at different temperatures (26°C, 30°C and 34°C), before being placed in nutrient-replete or -depleted seawater for 24 h. The corals were then incubated with 13C-labelled sodium bicarbonate and different 15N-labelled nitrogen forms (ammonium, urea and dissolved free amino acids) to determine their assimilation rates. We found that nutrient depletion inhibited the assimilation of all nitrogen sources studied and that heat stress reduced the assimilation of ammonium and dissolved free amino acids. However, the host assimilated over 3-fold more urea at 30°C relative to 26°C. Overall, both moderate heat stress (30°C) and nutrient depletion individually decreased the total nitrogen assimilated by the symbiont by 66%, and combined, they decreased assimilation by 79%. This led to the symbiotic algae becoming nitrogen starved, with the C:N ratio increasing by over 3-fold at 34°C, potentially exacerbating the impacts of coral bleaching.

Marine Bioluminescence: Simulation of Dynamics within a Pump-Through Bathyphotometer.

Bioluminescence is light produced by organisms through chemical reactions. In most cases, bioluminescent organisms produce light in response to mechanical stimulation, including from shear around objects moving in the water. Many phytoplankton and zooplankton are capable of producing bioluminescence, which is commonly measured as bioluminescence potential, defined as mechanically stimulated light measured inside of a chambered pump-through bathyphotometer. We have developed a numerical model of a pump-through bathyphotometer and simulated flow using Lagrangian particles as an approximation for bioluminescent marine plankton taxa. The results indicate that all particles remain in the detection chamber for a residence time of at least 0.25 s. This suggests that the total first flash of bioluminescent autotrophic and heterotrophic dinoflagellates will be measured based on the existing literature regarding their flash duration. We have found low sensitivity of particle residence time to variations in particle size, density, or measurement depth. In addition, the results show that a high percentage of organisms may experience stimulation well before the detection chamber, or even multiple stimulations within the detection chamber. The results of this work serve to inform the processing of current bioluminescent potential data and assist in the development of future instruments.

Response of the toxic dinoflagellate Alexandrium minutum to exudates of the eelgrass Zostera marina.

Biotic interactions are a key factor in the development of harmful algal blooms. Recently, a lower abundance of planktonic dinoflagellates has been reported in areas dominated by seagrass beds, suggesting a negative interaction between both groups of organisms. The interaction between planktonic dinoflagellates and marine phanerogams, as well as the way in which bacteria can affect this interaction, was studied in two experiments using a non-axenic culture of the toxic dinoflagellate Alexandrium minutum exposed to increasing additions of eelgrass (Zostera marina) exudates from old and young leaves and to the presence or absence of antibiotics. In these experiments, A. minutum abundance, growth rate and photosynthetic efficiency (Fv/Fm), as well as bacterial abundance, were measured every 48 h. Toxin concentration per cell was determined at the end of both experiments. Our results demonstrated that Z. marina exudates reduced A. minutum growth rate and, in one of the experiments, also the photosynthetic efficiency. These results are not an indirect effect mediated by the bacteria in the culture, although their growth modify the magnitude of the negative impact on the dinoflagellate growth rate. No clear pattern was observed in the variation of toxin production with the treatments.

Revealing the algicidal characteristics of Maribacter dokdonensis: An investigation into bacterial strain P4 isolated from Karenia mikimotoi bloom water.

Harmful algal blooms (HABs) are a global environmental concern, causing significant economic losses in fisheries and posing risks to human health. Algicidal bacteria have been suggested as a potential solution to control HABs, but their algicidal efficacy is influenced by various factors. This study aimed to characterize a novel algicidal bacterium, Maribacter dokdonensis (P4), isolated from a Karenia mikimotoi (Hong Kong strain, KMHK) HAB and assess the impact of P4 and KMHK's doses, growth phase, and algicidal mode and the axenicity of KMHK on P4's algicidal effect. Our results demonstrated that the algicidal effect of P4 was dose-dependent, with the highest efficacy at a dose of 25% v/v. The study also determined that P4's algicidal effect was indirect, with the P4 culture and the supernatant, but not the bacterial cells, showing significant effects. The algicidal efficacy was higher when both P4 and KMHK were in the stationary phase. Furthermore, the P4 culture at the log phase could effectively kill KMHK cells at the stationary phase, with higher algicidal efficacy in the bacterial culture than that of the supernatant alone. Interestingly, P4's algicidal efficacy was significantly higher when co-culturing with xenic KMHK (~90% efficacy at day 1) than that with the axenic KMHK (~50% efficacy at day 1), suggesting the presence of other bacteria could regulate P4's algicidal effect. The bacterial strain P4 also exhibited remarkable algicidal efficacy on four other dinoflagellate species, particularly the armored species. These results provide valuable insights into the algicidal effect of M. dokdonensis on K. mikimotoi and on their interactions.

A laboratory study of the increasing competitiveness of Karenia mikimotoi under rising CO2 scenario.

Ocean acidification (OA) driven by elevated carbon dioxide (CO2) levels is expected to disturb marine ecological processes, including the formation and control of harmful algal blooms (HABs). In this study, the effects of rising CO2 on the allelopathic effects of macroalgae Ulva pertusa to a toxic dinoflagellate Karenia mikimotoi were investigated. It was found that high level of CO2 (1000 ppmv) promoted the competitive growth of K. mikimotoi compared to the group of present ambient CO2 level (420ppmv), with the number of algal cell increased from 32.2 × 104 cells/mL to 36.75 × 104 cells/mL after 96 h mono-culture. Additionally, rising CO2 level weakened allelopathic effects of U. pertusa on K. mikimotoi, as demonstrated by the decreased inhibition rate (50.6 % under the original condition VS 34.3 % under the acidified condition after 96 h co-culture) and the decreased reactive oxygen species (ROS) level, malondialdehyde (MDA) content, antioxidant enzymes activity (superoxide dismutase (SOD), peroxidase (POD), glutathione peroxidase (GPX), glutathione reductase (GR) and catalase (CAT) and non-enzymatic antioxidants (glutathione (GSH) and ascorbic acid (ascorbate, vitamin C). Indicators for cell apoptosis of K. mikimotoi including decreased caspase-3 and -9 protease activity were observed when the co-cultured systems were under rising CO2 exposure. Furthermore, high CO2 level disturbed fatty acid synthesis in U. pertusa and significantly decreased the contents of fatty acids with allelopathy, resulting in the allelopathy weakening of U. pertusa. Collectively, rising CO2 level promoted the growth of K. mikimotoi and weakened allelopathic effects of U. pertusa on K. mikimotoi, indicating the increased difficulties in controlling K. mikimotoi using macroalgae in the future.

Unveiling the evolution of phytoplankton communities: Decades-long insights into the southern Yellow Sea, China (1959-2023).

We obtained historical and observational data on phytoplankton communities from 1959 to 2023 to explore the responses of the phytoplankton community structure to long-term environmental changes in the southern Yellow Sea (SYS), China. The results revealed a decrease in the proportions of diatom cell abundance within the phytoplankton community by 8 %, accompanied by a corresponding increase in that of dinoflagellates. Dominant phytoplankton species were mainly chain-forming diatoms before 2000, and large dinoflagellate species from the genera Tripos and Noctiluca increased their dominance after 2000. Warm-water phytoplankton species have increased in dominance over the study period. Correlation analysis revealed that the ocean warming and alterations in nutrient structure (N/P and Si/N ratios) were mostly responsible for the long-term evolution trend, and these changes may result in an increase in dinoflagellate harmful algal blooms, reduced efficiency of the biological carbon pump, and heightened hypoxia in the future, which should draw our attention.

Microplastics inhibit the growth of endosymbiotic Symbiodinium tridacnidorum by altering photosynthesis and bacterial community.

Microplastics, ubiquitous anthropogenic marine pollutants, represent potential threats to coral-Symbiodiniaceae relationships in global reef ecosystems. However, the mechanism underlying the impacts of polystyrene microplastics (PS-MPs) on Symbiodiniaceae remains poorly understood. In this study, the cytological, physiological, and microbial responses of Symbiodinium tridacnidorum, a representative Symbiodiniaceae species, to varying concentrations of PS-MPs (0, 5, 50, 100, and 200 mg L-1) were investigated. The results revealed that microplastic exposure inhibited cell division, resulting in reduced cell density compared to control group. Furthermore, algal photosynthetic activity, as indicated by chlorophyll content, Fv/Fm, and net photosynthetic rate, declined with increasing microplastic concentration up to 50 mg L-1. Notably, elevated levels of microplastics (100 and 200 mg L-1) prompted a significant increase in cell size in S. tridacnidorum. Transmission electron microscopy and fluorescence microscopy indicated that hetero-aggregation was formed between high levels of PS-MPs and algal cells, ultimately causing damage to S. tridacnidorum. Moreover, the impact of PS-MPs exposure on the bacterial community associated with S. tridacnidorum was investigated. The results showed a reduction in alpha diversity of the bacterial community in groups exposed to 50, 100, and 200 mg L-1 of microplastics compared to those treated with 0 and 5 mg L-1. Additionally, the relative abundance of Marinobacter, Marivita, and Filomicrobium significantly increased, while Algiphilus and norank Nannocystaceae declined after microplastic exposure. These findings suggest that MPs can inhibit the growth of S. tridacnidorum and alter the associated bacterial community, posing a potential serious threat to coral symbiosis involving S. tridacnidorum.

Host starvation and in hospite degradation of algal symbionts shape the heat stress response of the Cassiopea-Symbiodiniaceae symbiosis.

BACKGROUND: Global warming is causing large-scale disruption of cnidarian-Symbiodiniaceae symbioses fundamental to major marine ecosystems, such as coral reefs. However, the mechanisms by which heat stress perturbs these symbiotic partnerships remain poorly understood. In this context, the upside-down jellyfish Cassiopea has emerged as a powerful experimental model system. RESULTS: We combined a controlled heat stress experiment with isotope labeling and correlative SEM-NanoSIMS imaging to show that host starvation is a central component in the chain of events that ultimately leads to the collapse of the Cassiopea holobiont. Heat stress caused an increase in catabolic activity and a depletion of carbon reserves in the unfed host, concurrent with a reduction in the supply of photosynthates from its algal symbionts. This state of host starvation was accompanied by pronounced in hospite degradation of algal symbionts, which may be a distinct feature of the heat stress response of Cassiopea. Interestingly, this loss of symbionts by degradation was concealed by body shrinkage of the starving animals, resulting in what could be referred to as "invisible" bleaching. CONCLUSIONS: Overall, our study highlights the importance of the nutritional status in the heat stress response of the Cassiopea holobiont. Compared with other symbiotic cnidarians, the large mesoglea of Cassiopea, with its structural sugar and protein content, may constitute an energy reservoir capable of delaying starvation. It seems plausible that this anatomical feature at least partly contributes to the relatively high stress tolerance of these animals in rapidly warming oceans. Video Abstract.

Starvation differentially affects gene expression, immunity and pathogen susceptibility across symbiotic states in a model cnidarian.

Mutualistic symbioses between cnidarians and photosynthetic algae are modulated by complex interactions between host immunity and environmental conditions. Here, we investigate how symbiosis interacts with food limitation to influence gene expression and stress response programming in the sea anemone Exaiptasia pallida (Aiptasia). Transcriptomic responses to starvation were similar between symbiotic and aposymbiotic Aiptasia; however, aposymbiotic anemone responses were stronger. Starved Aiptasia of both symbiotic states exhibited increased protein levels of immune-related transcription factor NF-κB, its associated gene pathways, and putative target genes. However, this starvation-induced increase in NF-κB correlated with increased immunity only in symbiotic anemones. Furthermore, starvation had opposite effects on Aiptasia susceptibility to pathogen and oxidative stress challenges, suggesting distinct energetic priorities under food scarce conditions. Finally, when we compared starvation responses in Aiptasia to those of a facultative coral and non-symbiotic anemone, 'defence' responses were similarly regulated in Aiptasia and the facultative coral, but not in the non-symbiotic anemone. This pattern suggests that capacity for symbiosis influences immune responses in cnidarians. In summary, expression of certain immune pathways-including NF-κB-does not necessarily predict susceptibility to pathogens, highlighting the complexities of cnidarian immunity and the influence of symbiosis under varying energetic demands.

Effects of culture conditions on the growth of the benthic dinoflagellates Ostreopsis cf. ovata, Prorocentrum lima and Coolia malayensis (Dinophyceae): A global review.

Benthic dinoflagellates produce potent toxins that may negatively affect humans and the marine biota. Understanding the factors that stimulate their growth is important for management strategies and to reduce their potential negative impacts. Laboratory cultures have been extensively used to study microalgae physiology and characterize life cycles, nutrition, growth rates, among other processes. A systematic review of the literature on the growth parameters of the benthic dinoflagellates Ostreopsis cf. ovata, Prorocentrum lima species complex and Coolia malayensis obtained in laboratory cultures of strains isolated from all over the world was performed. The effects of temperature, light intensity, photoperiod, salinity and culture media on the growth rate of these species were evaluated using multiple regressions and a model selection approach, based on the Akaike Information Criteria (AIC). The potential effects of the initial culture abundance and the media volume used on the growth of the species were also assessed. Data from 50 articles (25 for O. cf. ovata, 21 for P. lima and 6 for C. malayensis), resulting in 399 growth parameter values (growth rate, doubling time and maximum yield) were compiled in a database. The genetic clades of O. cf. ovata and P. lima species complex were also noted. Growth rate was the most frequently reported growth parameter for the three species, and 127 values were retrieved for O. cf. ovata, 90 for P. lima and 56 for C. malayensis. Temperature was the factor that best explained the growth response of P. lima and C. malayensis, whereas for O. cf. ovata, temperature and salinity were equally important. Light intensity and photoperiod were included among the six best models for the studied species but presented a weaker effect on growth. Given the observed and future projected climate change, increasing ocean temperature will promote the growth of these species, likely leading to an expansion of their impacts on ecosystems and human health. The use of common garden experiments using multiple strains from different geographic domains, particularly addressing underrepresented lineages is recommended, as they will provide more balanced insight regarding the species physiological responses to environmental drivers.

Comparative physiology reveals heat stress disrupts acid-base homeostasis independent of symbiotic state in the model cnidarian Exaiptasia diaphana.

Climate change threatens the survival of symbiotic cnidarians by causing photosymbiosis breakdown in a process known as bleaching. Direct effects of temperature on cnidarian host physiology remain difficult to describe because heatwaves depress symbiont performance, leading to host stress and starvation. The symbiotic sea anemone Exaiptasia diaphana provides an opportune system to disentangle direct versus indirect heat effects on the host, as it can survive indefinitely without symbionts. We tested the hypothesis that heat directly impairs cnidarian physiology by comparing symbiotic and aposymbiotic individuals of two laboratory subpopulations of a commonly used clonal strain of E. diaphana, CC7. We exposed anemones to a range of temperatures (ambient, +2°C, +4°C and +6°C) for 15-18 days, then measured their symbiont population densities, autotrophic carbon assimilation and translocation, photosynthesis, respiration and host intracellular pH (pHi). Symbiotic anemones from the two subpopulations differed in size and symbiont density and exhibited distinct heat stress responses, highlighting the importance of acclimation to different laboratory conditions. Specifically, the cohort with higher initial symbiont densities experienced dose-dependent symbiont loss with increasing temperature and a corresponding decline in host photosynthate accumulation. In contrast, the cohort with lower initial symbiont densities did not lose symbionts or assimilate less photosynthate when heated, similar to the response of aposymbiotic anemones. However, anemone pHi decreased at higher temperatures regardless of cohort, symbiont presence or photosynthate translocation, indicating that heat consistently disrupts cnidarian acid-base homeostasis independent of symbiotic status or mutualism breakdown. Thus, pH regulation may be a critical vulnerability for cnidarians in a changing climate.

Triggers, cascades, and endpoints: connecting the dots of coral bleaching mechanisms.

The intracellular coral-dinoflagellate symbiosis is the engine that underpins the success of coral reefs, one of the most diverse ecosystems on the planet. However, the breakdown of the symbiosis and the loss of the microalgal symbiont (i.e. coral bleaching) due to environmental changes are resulting in the rapid degradation of coral reefs globally. There is an urgent need to understand the cellular physiology of coral bleaching at the mechanistic level to help develop solutions to mitigate the coral reef crisis. Here, at an unprecedented scope, we present novel models that integrate putative mechanisms of coral bleaching within a common framework according to the triggers (initiators of bleaching, e.g. heat, cold, light stress, hypoxia, hyposalinity), cascades (cellular pathways, e.g. photoinhibition, unfolded protein response, nitric oxide), and endpoints (mechanisms of symbiont loss, e.g. apoptosis, necrosis, exocytosis/vomocytosis). The models are supported by direct evidence from cnidarian systems, and indirectly through comparative evolutionary analyses from non-cnidarian systems. With this approach, new putative mechanisms have been established within and between cascades initiated by different bleaching triggers. In particular, the models provide new insights into the poorly understood connections between bleaching cascades and endpoints and highlight the role of a new mechanism of symbiont loss, i.e. 'symbiolysosomal digestion', which is different from symbiophagy. This review also increases the approachability of bleaching physiology for specialists and non-specialists by mapping the vast landscape of bleaching mechanisms in an atlas of comprehensible and detailed mechanistic models. We then discuss major knowledge gaps and how future research may improve the understanding of the connections between the diverse cascade of cellular pathways and the mechanisms of symbiont loss (endpoints).

Evolutionary radiation and microbial community dynamics shape the thermal tolerance of Fungiidae in the southern South China Sea.

Fungiidae have shown increased thermal adaptability in coral reef ecosystems under global warming. This study analyzes the evolutionary divergence and microbial communities of Fungiidae in the Sanjiao Reef of the southern South China Sea and explores the impact of coral evolution radiation and microbial dynamics on the heat tolerance of Fungiidae. The results found that Cycloseris was an ancient branch of Fungiidae, dating back approximately 147.8953 Mya, and Fungiidae differentiated into two ancestral clades (clades I and II) before 107.0312 Ma. Fungiidae exhibited specific symbioses with the Cladocopium C27 sub-clade. Notably, the Cladocopium C1 sub-clade has a high relative abundance in clade I, whereas the heat-tolerant Cladocopium C40 and C3u sub-clades subdominante in clade II. Regarding bacterial communities, Cycloseris costulata, the earliest divergent species, had higher bacterial ß-diversity, while the latest divergent species, Lithophyllon scabra, displayed lower bacterial α-diversity and higher community stability. Beneficial bacteria dominante Fungiidae's bacterial community (54%). The co-occurrence network revealed that microbial networks in clade II exhibited lower complexity and greater resilience than those in clade I. Our study highlights that host evolutionary radiation and microbial communities shaped Fungiidae's thermal tolerance. The variability in subdominant Symbiodiniaceae populations may contribute to interspecific differences in thermal tolerance along the evolutionary branches of Fungiidae. The presence of abundant beneficial bacteria may further enhance the thermal ability of the Fungiidae. Furthermore, the later divergent species of Fungiidae have stronger heat tolerance, possibly driven by the increased regulation ability of the host on the bacterial community, greater microbial community stability, and interaction network resistance.IMPORTANCECoral reefs are facing significant threats due to global warming. The heat tolerance of coral holobionts depends on both the coral host and its microbiome. However, the association between coral evolutionary radiation and interspecific differences in microbial communities remains unclear. In this study, we investigated the role of evolutionary radiation and microbial community dynamics in shaping the thermal acclimation potential of Fungiidae in the Sanjiao Reef of the southern South China Sea. The study's results suggest that evolutionary radiation enhances the thermal tolerance of Fungiidae. Fungiidae species that have diverged more recently have exhibited a higher presence of heat-tolerant Symbiodiniaceae taxa, more stable bacterial communities, and a robust and resilient microbial interaction network, improving the thermal adaptability of Fungiidae. In summary, this study provides new insights into the thermal adaptation patterns of corals under global warming conditions.