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Abstract Transcription factor nuclear factor-kappa B (NF-κB) and many upstream signaling components have been identified in a diversity of holozoan taxa, including unicellular holozoans (eg Filasterea and Choanoflagellata) and the metazoan phyla Porifera (sponges), Placozoa, and Cnidaria (eg jellyfishes, sea anemones, corals, and hydra). Herein, we review recent progress made toward characterizing the structure, regulation, activity, and biological functions of NF-κB proteins found in these taxa. We also provide an updated phylogenetic sampling of NF-κB orthologs highlighting their different domain configurations among holozoans, as well as a method for comparing the computationally predicted three-dimensional structures of NF-κB dimers and relating these structures to their amino acid similarities and DNA-binding specificities. This synthesis reveals new insights regarding the evolutionarily conserved and variable domain-dependent activities and regulation of holozoan NF-κBs. Further, we provide an overview of the roles of NF-κB in pathogen responses, stress responses, symbiosis, and development, with a focus on recent findings from sponges and cnidarians. This curation of a growing body of knowledge highlights both conserved and divergent roles of NF-κB in foundational biological processes. Finally, we suggest priorities for future research on the evolution of NF-κB structure and function. Overall, investigations of NF-κB in diverse holozoan taxa will continue to provide information about the origins of this important and pervasive transcriptional regulator and will also contribute to an understanding of the responses of sentinel species to the modern-day stresses associated with changing environmental conditions and novel pathogen-based diseases. 

Heat stress can disrupt acid–base homeostasis in reef-building corals and other tropical cnidarians, often leading to cellular acidosis that can undermine organismal function. Temperate cnidarians experience a high degree of seasonal temperature variability, leading us to hypothesize that temperate taxa have more thermally robust pH homeostasis than their tropical relatives. To test this, we investigated how elevated temperature affects intracellular pH and calcification in the temperate coralAstrangia poculata. Clonal pairs were exposed to elevated (30°C) or control (22°C) temperatures for 17 days. Despite causing damage to host tissues and symbiont cells, elevated temperature did not affect intracellular pH or inhibit calcification inA. poculata. These responses contrast with those of tropical cnidarians, which experience cellular acidification and decreased growth during heat stress.Astrangia poculatatherefore appears to have thermally resilient cellular acid–base homeostasis mechanisms, possibly because of adaptation to large seasonal temperature variations. However, we also observed tissue damage and lower egg densities in heat-treated individuals, suggesting that increasingly severe marine heatwaves can still threaten temperate coral fitness. These results provide insight into corals’ nuanced adaptive capacity across latitudes and biological scales. 

Anthropogenic pollution is driving an increase in the frequency and severity of seawater hypoxic events in coastal marine ecosystems. Although hypoxia decreases physiological performance in coral and sea anemone (phylum Cnidaria) larvae, the underlying cellular mechanisms remain unexplored. Here, larvae of the reef-building corals Galaxea fascicularis and Porites astreoides and the estuarine sea anemone Nematostella vectensis were exposed to normoxia or a simulated hypoxic event (6 h at <2 mg dissolved O2 l−1), and their metabolomic response was quantified at the end of the exposure period using targeted liquid chromatography-mass spectrometry. Baseline metabolite profiles (81 amino acids, acylcarnitines, organic acids and nucleotides) were broadly divergent between the three species, with the corals displaying a reliance on nitrogen cycling through amino acid metabolism, whereas N. vectensis relied on nucleotide metabolism. By contrast, several changes in metabolite abundances under hypoxia were shared (e.g. increases in lactate) and suggest the upregulation of glycolysis, lactic acid fermentation and fatty acid β-oxidation as conserved mechanisms for energy production under hypoxia. Changes in these pathways were correlated with adverse physiological outcomes, including conserved declines in swimming behavior and growth. Importantly, life history traits affecting metabolism influenced hypoxia responses. For example, P. astreoides larvae, which possess algal endosymbionts, displayed the least severe metabolic response to hypoxia among these species, possibly owing to symbiont resources. Overall, these findings demonstrate that hypoxia disrupts metabolic performance in coral and sea anemone larvae through conserved and divergent pathways, emphasizing the need to limit drivers of ocean deoxygenation. 

Seawater hypoxia is increasing globally and can drive declines in organismal performance across a wide range of marine taxa. However, the effects of hypoxia on early life stages (e.g., larvae and juveniles) are largely unknown, and it is unclear how evolutionary and life histories may influence these outcomes. Here, we addressed this question by comparing hypoxia responses across early life stages of three cnidarian species representing a range of life histories: the reef‐building coralGalaxea fascicularis, a broadcast spawner with horizontal transmission of endosymbiotic algae (family Symbiodiniaceae); the reef‐building coralPorites astreoides, a brooder with vertical endosymbiont transmission; and the estuarine sea anemoneNematostella vectensis, a non‐symbiotic broadcast spawner. Transient exposure of larvae to hypoxia (dissolved oxygen < 2 mg L⁻¹for 6 h) led to decreased larval swimming and growth for all three species, which resulted in impaired settlement for the corals. Coral‐specific responses also included larval swelling, depressed respiration rates, and decreases in symbiont densities and function. These results indicate both immediate and latent negative effects of hypoxia on cnidarian physiology and coral–algal mutualisms specifically. In addition,G. fascicularisandP. astreoideswere sensitized to heat stress following hypoxia exposure, suggesting that the combinatorial nature of climate stressors will lead to declining performance for corals. However, sensitization to heat stress was not observed inN. vectensisexposed to hypoxia, suggesting that this species may be more resilient to combined stressors. Overall, these results emphasize the importance of reducing anthropogenic carbon emissions to limit further ocean deoxygenation and warming. 

ABSTRACT During the 4th Global Coral Bleaching Event (GCBE4; January 2023–September 2025), an extreme marine heatwave occurred on the Bocas del Toro Reef Complex (BTRC) in Panama. We characterized how this heatwave impacted the health and holobiont communities of the stress‐tolerant coralSiderastrea sidereaat four sites across the BTRC. Tagged colonies at each site (N = 30–53 colonies per site) were visited before, during, and after the heatwave (early May 2022, mid‐August 2023, and late April 2024, respectively), and images and DNA samples were collected at each time point. In situ temperature logger data showed that sites reached maxima of 32.1°C–33.9°C in October 2023, resulting in the accumulation of ~12–20 maximum degree‐heating weeks (DHWs). Consequently,S. sidereacolonies displayed widespread bleaching (i.e., the loss of algal endosymbionts), with an increase from 8.6% to 33% of colonies bleached per site in May 2022 to 33%–70% in August 2023, followed by a decline to 15%–63% by April 2024. Colony‐level partial mortality increased significantly between 2022 and 2024 at three of the four sites, and was observed even in colonies that were not bleached in August 2023. Further, many corals hostingCladocopiumspp. algal symbionts in 2022 shifted towards less diverse communities dominated by heat‐tolerantBreviolumandDurusdiniumspp., and most of these corals continued to host modified symbiont communities for months. The heatwave also reshaped corals' bacterial microbiomes, including increases in α‐diversity and abundances of potentially pathogenic taxa (e.g., Vibrionaceae), and these shifts were persistent following the heatwave. Together, these findings demonstrate that GCBE4 had lasting impacts onS. sidereaholobiont health across the BTRC, underscoring that extreme heat events can compromise even stress‐tolerant coral species and induce legacy effects that will likely affect their future resilience. Rapid action to minimize further ocean warming is thus necessary to safeguard reef ecosystems. 

Most stony corals liberate their gametes into the water column via broadcast spawning, where fertilization hinges upon the activation of directional sperm motility. Sperm from gonochoric and hermaphroditic corals display distinct morphological and molecular phenotypes, yet it is unknown whether the signalling pathways controlling sperm motility are also distinct between these sexual systems. Here, we addressed this knowledge gap using the gonochoric, broadcast spawning coralAstrangia poculata. We found that cytosolic alkalinization of sperm activates the pH-sensing enzyme soluble adenylyl cyclase (sAC), which is required for motility. Additionally, we demonstrate for the first time in any cnidarian that sAC activity leads to protein kinase A (PKA) activation, and that PKA activity contributes to sperm motility activation. Ultrastructures ofA. poculatasperm displayed morphological homology with other gonochoric cnidarians, and sAC exhibited broad structural and functional conservation across this phylum. These results indicate a conserved role for pH-dependent sAC-cAMP-PKA signalling in sperm motility across coral sexual systems, and suggest that the role of this pathway in sperm motility may be ancestral in metazoans. Finally, the dynamics of this pH-sensitive pathway may play a critical role in determining the sensitivity of marine invertebrate reproduction to anthropogenic ocean acidification. 

Increasingly frequent marine heatwaves are devastating coral reefs. Corals that survive these extreme events must rapidly recover if they are to withstand subsequent events, and long-term survival in the face of rising ocean temperatures may hinge on recovery capacity and acclimatory gains in heat tolerance over an individual’s lifespan. To better understand coral recovery trajectories in the face of successive marine heatwaves, we monitored the responses of bleaching-susceptible and bleaching-resistant individuals of two dominant coral species in Hawai’i,Montipora capitataandPorites compressa, over a decade that included three marine heatwaves. Bleaching-susceptible colonies ofP. compressaexhibited beneficial acclimatization to heat stress (i.e., less bleaching) following repeat heatwaves, becoming indistinguishable from bleaching-resistant conspecifics during the third heatwave. In contrast, bleaching-susceptibleM. capitatarepeatedly bleached during all successive heatwaves and exhibited seasonal bleaching and substantial mortality for up to 3 y following the third heatwave. Encouragingly, bleaching-resistant individuals of both species remained pigmented across the entire time series; however, pigmentation did not necessarily indicate physiological resilience. Specifically,M. capitatadisplayed incremental yet only partial recovery of symbiont density and tissue biomass across both bleaching phenotypes up to 35 mo following the third heatwave as well as considerable partial mortality. Conversely,P. compressaappeared to recover across most physiological metrics within 2 y and experienced little to no mortality. Ultimately, these results indicate that even some visually robust, bleaching-resistant corals can carry the cost of recurring heatwaves over multiple years, leading to divergent recovery trajectories that may erode coral reef resilience in the Anthropocene. 

ABSTRACT Ocean acidification (OA) resulting from anthropogenic CO2 emissions is impairing the reproduction of marine organisms. While parental exposure to OA can protect offspring via carryover effects, this phenomenon is poorly understood in many marine invertebrate taxa. Here, we examined how parental exposure to acidified (pH 7.40) versus ambient (pH 7.72) seawater influenced reproduction and offspring performance across six gametogenic cycles (13 weeks) in the estuarine sea anemone Nematostella vectensis. Females exhibited reproductive plasticity under acidic conditions, releasing significantly fewer but larger eggs compared to ambient females after 4 weeks of exposure, and larger eggs in two of the four following spawning cycles despite recovering fecundity, indicating long-term acclimatization and greater investment in eggs. Males showed no changes in fecundity under acidic conditions but produced a greater percentage of sperm with high mitochondrial membrane potential (MMP; a proxy for elevated motility), which corresponded with higher fertilization rates relative to ambient males. Finally, parental exposure to acidic conditions did not significantly influence offspring development rates, respiration rates, or heat tolerance. Overall, this study demonstrates that parental exposure to acidic conditions impacts gamete production and physiology but not offspring performance in N. vectensis, suggesting that increased investment in individual gametes may promote fitness. 

Across diverse taxa, sublethal exposure to abiotic stressors early in life can lead to benefits such as increased stress tolerance upon repeat exposure. This phenomenon, known as hormetic priming, is largely unexplored in early life stages of marine invertebrates, which are increasingly threatened by anthropogenic climate change. To investigate this phenomenon, larvae of the sea anemone and model marine invertebrateNematostella vectensiswere exposed to control (18 °C) or elevated (24 °C, 30 °C, 35 °C, or 39 °C) temperatures for 1 h at 3 days post-fertilization (DPF), followed by return to control temperatures (18 °C). The animals were then assessed for growth, development, metabolic rates, and heat tolerance at 4, 7, and 11 DPF. Priming at intermediately elevated temperatures (24 °C, 30 °C, or 35 °C) augmented growth and development compared to controls or priming at 39 °C. Indeed, priming at 39 °C hampered developmental progression, with around 40% of larvae still in the planula stage at 11 DPF, in contrast to 0% for all other groups. Total protein content, a proxy for biomass, and respiration rates were not significantly affected by priming, suggesting metabolic resilience. Heat tolerance was quantified with acute heat stress exposures, and was significantly higher for animals primed at intermediate temperatures (24 °C, 30 °C, or 35 °C) compared to controls or those primed at 39 °C at all time points. To investigate a possible molecular mechanism for the observed changes in heat tolerance, the expression of heat shock protein 70 (HSP70) was quantified at 11 DPF. Expression of HSP70 significantly increased with increasing priming temperature, with the presence of a doublet band for larvae primed at 39 °C, suggesting persistent negative effects of priming on protein homeostasis. Interestingly, primed larvae in a second cohort cultured to 6 weeks post-fertilization continued to display hormetic growth responses, whereas benefits for heat tolerance were lost; in contrast, negative effects of short-term exposure to extreme heat stress (39 °C) persisted. These results demonstrate that some dose-dependent effects of priming waned over time while others persisted, resulting in heterogeneity in organismal performance across ontogeny following priming. Overall, these findings suggest that heat priming may augment the climate resilience of marine invertebrate early life stagesviathe modulation of key developmental and physiological phenotypes, while also affirming the need to limit further anthropogenic ocean warming. 

Coastal seawater hypoxia is increasing in temperate estuaries under global climate change, yet it is unknown how low oxygen conditions affect most estuarine species. We found that hypoxia has increased since the 1990s in an estuary hosting the sea anemoneNematostella vectensis(Jacques Cousteau National Estuarine Research Reserve, New Jersey, USA). AdultN. vectensisbred from anemones collected in this estuary exposed to three consecutive nights of hypoxia (dissolved oxygen = 0.5–1.5 mg L⁻¹for ~12 h night⁻¹) during gametogenesis displayed decreased aerobic respiration rates and biomass, indicating metabolic disruption. Physiological declines were correlated with changes in the expression of genes related to oxygen‐dependent metabolic processes, many of which are targets of hypoxia‐inducible factor 1α (HIF1α), demonstrating the activity of this transcription factor for the first time in this early‐diverging metazoan. The upregulation of genes involved in the unfolded protein response and endoplasmic reticulum and Golgi apparatus homeostasis suggested that misfolded proteins contributed to disrupted physiology. Notably, these responses were more pronounced in females, demonstrating sex‐specific sensitivity that was also observed in reproductive outcomes, with declines in female but not male fecundity following hypoxia exposure. However, sperm from exposed males had higher mitochondrial membrane potential, indicating altered spermatogenesis. Further, crosses performed with gametes from hypoxia‐exposed adults yielded strikingly low developmental success (~2%), yet larvae that did develop displayed similar respiration rates and accelerated settlement compared to controls. Overall, hypoxia depressed fitness inN. vectensisby over 95%, suggesting that even stress‐tolerant estuarine species may be threatened by coastal deoxygenation.