Characterizing environmental stress responses of aposymbiotic <i>Astrangia poculata</i> to divergent thermal challenges

Wuitchik, Daniel M.; Almanzar, Adeline; Benson, Brooke E.; Brennan, Sara A; Chavez, Juan D.; Liesegang, Mary B.; Reavis, Jennifer L.; Reyes, C.; Schniedewind, Mikaela K.; Trumble, Isabela F; Davies, Sarah W.

doi:10.1111/mec.16108

Cited by 25 publications

(39 citation statements)

References 97 publications

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“…These species tend to have sub-tropical distributions and can be found with extremely low symbiotic densities in the wild, especially at more northern latitudes, in low light environments, or in winter seasons 40 , 41 . Unlike other symbiosis models, such as Aiptasia or the upside-down jellyfish Cassiopea xamachana , facultative corals including Oculina arbuscula (this study) and Astrangia poculata (another emerging model species 42 – 44 ) calcify just as tropical reef-building corals do (Fig. 1 B).…”

Section: Introductionmentioning

confidence: 68%

“…Such comparisons have the potential to reveal direct genetic underpinnings and cellular mechanisms of symbiosis, which are challenging to disentangle in systems that exhibit natural variation in symbiotic densities. Future work on this and other facultative coral systems such as Astrangia poculata 44 , 102 or Oculina patagonica 103 , 104 will help elucidate the workings of a canonical and ecologically important endosymbiosis between reef-building corals and their dinoflagellate partners.…”

Section: Resultsmentioning

confidence: 99%

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Symbiosis maintenance in the facultative coral, Oculina arbuscula, relies on nitrogen cycling, cell cycle modulation, and immunity

Rivera

Davies

2021

Sci Rep

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Symbiosis with unicellular algae in the family Symbiodiniaceae is common across tropical marine invertebrates. Reef-building corals offer a clear example of cellular dysfunction leading to a dysbiosis that disrupts entire ecosystems in a process termed coral bleaching. Due to their obligate symbiotic relationship, understanding the molecular underpinnings that sustain this symbiosis in tropical reef-building corals is challenging, as any aposymbiotic state is inherently coupled with severe physiological stress. Here, we leverage the subtropical, facultatively symbiotic and calcifying coral Oculina arbuscula to investigate gene expression differences between aposymbiotic and symbiotic branches within the same colonies under baseline conditions. We further compare gene ontology (GO) and KOG enrichment in gene expression patterns from O. arbuscula with prior work in the sea anemone Exaiptasia pallida (Aiptasia) and the salamander Ambystoma maculatum—both of which exhibit endophotosymbiosis with unicellular algae. We identify nitrogen cycling, cell cycle control, and immune responses as key pathways involved in the maintenance of symbiosis under baseline conditions. Understanding the mechanisms that sustain a healthy symbiosis between corals and Symbiodiniaceae algae is of urgent importance given the vulnerability of these partnerships to changing environmental conditions and their role in the continued functioning of critical and highly diverse marine ecosystems.

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Section: Introductionmentioning

confidence: 68%

Section: Resultsmentioning

confidence: 99%

Symbiosis maintenance in the facultative coral, Oculina arbuscula, relies on nitrogen cycling, cell cycle modulation, and immunity

Rivera

Davies

2021

Sci Rep

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“…First, NF-κB and TRAF3 are coordinately induced to high levels in the stony elkhorn coral Acropora palmata following acute heat stress 55 ; and in Nv following 2’3’-cGAMP stimulation of the c-Gas-STING pathway 25 . Additionally, TRAF3 has been suggested to play a role in coral heat stress response 56,57 , and has been proposed to be a NF-κB target gene in heat-stressed E. pallida 58 . Therefore, our results provide a dataset to explore new gene network interactions, as well as leading to the identification of unannotated gene transcripts that are involved in the cnidarian immune system, some of which may be previously unknown anti-microbial agents.…”

Section: Discussionmentioning

confidence: 99%

“…and in Nv following 2'3'-cGAMP stimulation of the c-Gas-STING pathway Additionally, TRAF3 has been suggested to play a role in coral heat stress response56,57 …”

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confidence: 99%

Starvation Decreases Immunity and Immune Regulatory Factor NF-κB in the Starlet Sea Anemone Nematostella vectensis

Carrión

Desai

Brennan

et al. 2022

Preprint

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Lack of proper nutrition (malnutrition) or the complete absence of all food (starvation) have important consequences on the physiology of all organisms. In many cases, nutritional status affects immunity, but, for the most part, the relationship between nutrition and immunity has been limited to studies in vertebrates and terrestrial invertebrates. Herein, we describe a positive correlation between nutrition and immunity in the sea anemone Nematostella vectensis. Gene expression profiling of adult fed and starved anemones showed downregulation of many genes involved in nutrient metabolism and cellular respiration, as well as immune-related genes, in starved animals. Starved adult anemones also had reduced protein levels and DNA-binding activity of immunity-related transcription factor NF-κB. Starved juvenile anemones had increased sensitivity to bacterial infection and also had lower NF-κB protein levels, as compared to fed controls. Weighted Gene Correlation Network Analysis (WGCNA) revealed significantly correlated gene networks that were inversely associated with starvation. Based on the WGCNA and a reporter gene assay, we identified TRAF3 as a likely NF-κB target gene in N. vectensis. Overall, these experiments demonstrate a correlation between nutrition and immunity in a basal marine metazoan, and the results have implications for the survival of marine organisms as they encounter changing environments.

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“…They pull in their tentacles, form a puffed-up ring around their oral disc, do not respond to tactile stimulation, and do not actively feed. During quiescence there are also physiological shifts including lowered coral growth rates (Grace, 2017), polyp loss (Dimond et al ., 2013), and shifts in the coral transcriptome, associated with thermal stress and lowered motility (Wuitchik et al ., 2021). Additionally, the physiological costs of dormancy can last beyond winter into spring (Trumbauer et al , 2021).…”

Section: Introductionmentioning

confidence: 99%

Reshuffling of the coral microbiome during dormancy

Brown

Sharp

Apprill

2022

Preprint

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Quiescence, or dormancy, is a response to stressful conditions in which an organism slows or halts physiological functioning. Although most species that undergo dormancy maintain complex microbiomes, there is little known about how dormancy influences and is influenced by the host’s microbiome, including in the temperate coral, Astrangia poculata. Northern populations of A. poculata undergo winter quiescence. Here, we characterized wild A. poculata microbiomes in a high-resolution sampling time series before, during, and after quiescence using 16S ribosomal RNA gene sequencing on active (RNA) and present (DNA) microbiomes. We observed a restructuring of the coral microbiome during quiescence that persisted after re-emergence. Upon entering quiescence, corals shed copiotrophic microbes, including putative pathogens, suggesting removal of these taxa as corals cease normal functioning. During and after quiescence, bacteria and archaea associated with nitrification were enriched, suggesting the quiescent microbiome may replace essential functions through supplying nitrate to corals and/or microbes. Overall, this study demonstrates that key microbial groups related to quiescence in A. poculata may play a role in the onset or emergence from dormancy, and long-term regulation of the microbiome composition. The predictability of dormancy in A. poculata provides an ideal natural manipulation system to further identify factors that regulate host-microbial associations.

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Characterizing environmental stress responses of aposymbiotic Astrangia poculata to divergent thermal challenges

Cited by 25 publications

References 97 publications

Symbiosis maintenance in the facultative coral, Oculina arbuscula, relies on nitrogen cycling, cell cycle modulation, and immunity

Symbiosis maintenance in the facultative coral, Oculina arbuscula, relies on nitrogen cycling, cell cycle modulation, and immunity

Starvation Decreases Immunity and Immune Regulatory Factor NF-κB in the Starlet Sea Anemone Nematostella vectensis

Reshuffling of the coral microbiome during dormancy

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