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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 anemoneExaiptasia 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.

 

Lack of proper nutrition has important consequences for the physiology of all organisms, and nutritional status can affect immunity, based on many studies in terrestrial animals. Here we show a positive correlation between nutrition and immunity in the sea anemoneNematostella vectensis. Gene expression profiling of adult anemones shows downregulation of genes involved in nutrient metabolism, cellular respiration, and immunity in starved animals. Starved adult anemones also have reduced protein levels and activity of immunity transcription factor NF-κB. Starved juvenile anemones have increased sensitivity to bacterial infection and also have lower NF-κB protein levels, as compared to fed controls. Weighted Gene Correlation Network Analysis (WGCNA) is used to identify significantly correlated gene networks that were downregulated with starvation. These experiments demonstrate a correlation between nutrition and immunity in an early diverged marine metazoan, and the results have implications for the survival of marine organisms as they encounter changing environments.

 

Heterotrophy has been shown to mitigate coral–algal dysbiosis (coral bleaching) under heat challenge, but the molecular mechanisms underlying this phenomenon remain largely unexplored. Here, we quantified coral physiology and gene expression of fragments from 13 genotypes of symbiotic Oculina arbuscula after a 28-d feeding experiment under (1) fed, ambient (24 °C); (2) unfed, ambient; (3) fed, heated (ramp to 33 °C); and (4) unfed, heated treatments. We monitored algal photosynthetic efficiency throughout the experiment, and after 28 d, profiled coral and algal carbohydrate and protein reserves, coral gene expression, algal cell densities, and chlorophyll-a and chlorophyll-c2 pigments. Contrary to previous findings, heterotrophy did little to mitigate the impacts of temperature, and we observed few significant differences in physiology between fed and unfed corals under heat challenge. Our results suggest the duration and intensity of starvation and thermal challenge play meaningful roles in coral energetics and stress response; future work exploring these thresholds and how they may impact coral responses under changing climate is urgently needed. Gene expression patterns under heat challenge in fed and unfed corals showed gene ontology enrichment patterns consistent with classic signatures of the environmental stress response. While gene expression differences between fed and unfed corals under heat challenge were subtle: Unfed, heated corals uniquely upregulated genes associated with cell cycle functions, an indication that starvation may induce the previously described, milder “type B” coral stress response. Future studies interested in disentangling the influence of heterotrophy on coral bleaching would benefit from leveraging the facultative species studied here, but using the coral in its symbiotic and aposymbiotic states.

 

Increasing ocean temperatures are causing dysbiosis between coral hosts and their symbionts. Previous work suggests that coral host gene expression responds more strongly to environmental stress compared to their intracellular symbionts; however, the causes and consequences of this phenomenon remain untested. We hypothesized that symbionts are less responsive because hosts modulate symbiont environments to buffer stress. To test this hypothesis, we leveraged the facultative symbiosis between the scleractinian coralOculina arbusculaand its symbiontBreviolum psygmophilumto characterize gene expression responses of both symbiotic partners in and ex hospite under thermal challenges. To characterize host and in hospite symbiont responses, symbiotic and aposymbioticO. arbusculawere exposed to three treatments: (1) control (18°C), (2) heat (32°C), and (3) cold (6°C). This experiment was replicated withB. psygmophilumcultured fromO. arbusculato characterize ex hospite symbiont responses. Both thermal challenges elicited classic environmental stress responses (ESRs) inO. arbuscularegardless of symbiotic state, with hosts responding more strongly to cold challenge. Hosts also exhibited stronger responses than in hospite symbionts. In and ex hospiteB. psygmophilumboth down‐regulated gene ontology pathways associated with photosynthesis under thermal challenge; however, ex hospite symbionts exhibited greater gene expression plasticity and differential expression of genes associated with ESRs. Taken together, these findings suggest thatO. arbusculahosts may buffer environments ofB. psygmophilumsymbionts; however, we outline the future work needed to confirm this hypothesis.

 

Tropical corals construct the three-dimensional framework for one of the most diverse ecosystems on the planet, providing habitat to a plethora of species across taxa. However, these ecosystem engineers are facing unprecedented challenges, such as increasing disease prevalence and marine heatwaves associated with anthropogenic global change. As a result, major declines in coral cover and health are being observed across the world's oceans, often due to the breakdown of coral-associated symbioses. Here, we review the interactions between the major symbiotic partners of the coral holobiont—the cnidarian host, algae in the family Symbiodiniaceae, and the microbiome—that influence trait variation, including the molecular mechanisms that underlie symbiosis and the resulting physiological benefits of different microbial partnerships. In doing so, we highlight the current framework for the formation and maintenance of cnidarian–Symbiodiniaceae symbiosis, and the role that immunity pathways play in this relationship. We emphasize that understanding these complex interactions is challenging when you consider the vast genetic variation of the cnidarian host and algal symbiont, as well as their highly diverse microbiome, which is also an important player in coral holobiont health. Given the complex interactions between and among symbiotic partners, we propose several research directions and approaches focused on symbiosis model systems and emerging technologies that will broaden our understanding of how these partner interactions may facilitate the prediction of coral holobiont phenotype, especially under rapid environmental change.

 

ABSTRACT In July 2016, a severe coral reef invertebrate mortality event occurred approximately 200 km southeast of Galveston, Texas, at the East Flower Garden Bank, wherein ∼82% of corals in a 0.06-km 2 area died. Based on surveys of dead corals and other invertebrates shortly after this mortality event, responders hypothesized that localized hypoxia was the most likely direct cause. However, no dissolved oxygen data were available to test this hypothesis, because oxygen is not continuously monitored within the Flower Garden Banks sanctuary. Here, we quantify microbial plankton community diversity based on four cruises over 2 years at the Flower Garden Banks, including a cruise just 5 to 8 days after the mortality event was first observed. In contrast with observations collected during nonmortality conditions, microbial plankton communities in the thermocline were differentially enriched with taxa known to be active and abundant in oxygen minimum zones or that have known adaptations to oxygen limitation shortly after the mortality event (e.g., SAR324, Thioglobaceae , Nitrosopelagicus , and Thermoplasmata MGII). Unexpectedly, these enrichments were not localized to the East Bank but were instead prevalent across the entire study area, suggesting there was a widespread depletion of dissolved oxygen concentrations in the thermocline around the time of the mortality event. Hydrographic analysis revealed the southern East Bank coral reef (where the localized mortality event occurred) was uniquely within the thermocline at this time. Our results demonstrate how temporal monitoring of microbial communities can be a useful tool to address questions related to past environmental events. IMPORTANCE In the northwestern Gulf of Mexico in July 2016, ∼82% of corals in a small area of the East Flower Garden Bank coral reef suddenly died without warning. Oxygen depletion is believed to have been the cause. However, there was considerable uncertainty, as no oxygen data were available from the time of the event. Microbes are sensitive to changes in oxygen and can be used as bioindicators of oxygen loss. In this study, we analyze microbial communities in water samples collected over several years at the Flower Garden Banks, including shortly after the mortality event. Our findings indicate that compared to normal conditions, oxygen depletion was widespread in the deep-water layer during the mortality event. Hydrographic analysis of water masses further revealed some of this low-oxygen water likely upwelled onto the coral reef. 

Rising atmospheric CO 2 reduces seawater pH causing ocean acidification (OA). Understanding how resilient marine organisms respond to OA may help predict how community dynamics will shift as CO 2 continues rising. The common slipper shell snail Crepidula fornicata is a marine gastropod native to eastern North America that has been a successful invader along the western European coastline and elsewhere. It has also been previously shown to be resilient to global change stressors. To examine the mechanisms underlying C. fornicata’s resilience to OA, we conducted two controlled laboratory experiments. First, we examined several phenotypes and genome-wide gene expression of C. fornicata in response to pH treatments (7.5, 7.6, and 8.0) throughout the larval stage and then tested how conditions experienced as larvae influenced juvenile stages (i.e., carry-over effects). Second, we examined genome-wide gene expression patterns of C. fornicata larvae in response to acute (4, 10, 24, and 48 h) pH treatment (7.5 and 8.0). Both C. fornicata larvae and juveniles exhibited resilience to OA and their gene expression responses highlight the role of transcriptome plasticity in this resilience. Larvae did not exhibit reduced growth under OA until they were at least 8 days old. These phenotypic effects were preceded by broad transcriptomic changes, which likely served as an acclimation mechanism for combating reduced pH conditions frequently experienced in littoral zones. Larvae reared in reduced pH conditions also took longer to become competent to metamorphose. In addition, while juvenile sizes at metamorphosis reflected larval rearing pH conditions, no carry-over effects on juvenile growth rates were observed. Transcriptomic analyses suggest increased metabolism under OA, which may indicate compensation in reduced pH environments. Transcriptomic analyses through time suggest that these energetic burdens experienced under OA eventually dissipate, allowing C. fornicata to reduce metabolic demands and acclimate to reduced pH. Carry-over effects from larval OA conditions were observed in juveniles; however, these effects were larger for more severe OA conditions and larvae reared in those conditions also demonstrated less transcriptome elasticity. This study highlights the importance of assessing the effects of OA across life history stages and demonstrates how transcriptomic plasticity may allow highly resilient organisms, like C. fornicata , to acclimate to reduced pH environments. 

Terrestrial runoff can negatively impact marine ecosystems through stressors including excess nutrients, freshwater, sediments, and contaminants. Severe storms, which are increasing with global climate change, generate massive inputs of runoff over short timescales (hours to days); such runoff impacted offshore reefs in the northwest Gulf of Mexico (NW GoM) following severe storms in 2016 and 2017. Several weeks after coastal flooding from these events, NW GoM reef corals, sponges, and other benthic invertebrates ∼185 km offshore experienced mortality (2016 only) and/or sub-lethal stress (both years). To assess the impact of storm-derived runoff on reef filter feeders, we characterized the bacterial communities of two sponges, Agelas clathrodes and Xestospongia muta , from offshore reefs during periods of sub-lethal stress and no stress over a three-year period (2016—2018). Sponge-associated and seawater-associated bacterial communities were altered during both flood years. Additionally, we found evidence of wastewater contamination (based on 16S rRNA gene libraries and quantitative PCR) in offshore sponge samples, but not in seawater samples, following these flood years. Signs of wastewater contamination were absent during the no-flood year. We show that flood events from severe storms have the capacity to reach offshore reef ecosystems and impact resident benthic organisms. Such impacts are most readily detected if baseline data on organismal physiology and associated microbiome composition are available. This highlights the need for molecular and microbial time series of benthic organisms in near- and offshore reef ecosystems, and the continued mitigation of stormwater runoff and climate change impacts.