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The resilience of coral reefs in oligotrophic, (sub)tropical oceans is largely due to the symbiotic relationship between scleractinian corals and Symbiodiniaceae algae, which enables efficient internal nutrient recycling. Investigating the history of this coral symbiosis can provide insights into its role in sustaining the health of both present and future coral reefs. The isotopic composition of organic nitrogen (15N/14N or δ15N) bound within coral skeletons has been utilized to trace the existence of symbiosis in fossil corals, suggesting that coral symbiosis dates back to at least 210 million years ago. The basis of this proxy is that symbiotic corals are expected to exhibit lower δ15N compared to their non-symbiotic (aposymbiotic) counterparts within the same environments, owing to internal nitrogen recycling between the coral host and algal symbiont, and reduced leakage of low-δ15N ammonium into seawater. However, this hypothesis has not been adequately tested in contemporary settings. In a laboratory experiment, we examined the δ15N differences between the symbiotic and aposymbiotic branches within the same genetic backgrounds of the facultatively symbiotic coralOculina arbusculaunder well-fed conditions. Across five different genotypes in two separate experiments, symbiotic branches consistently showed lower δ15N than their aposymbiotic counterparts. These findings corroborate the use of δ15N as a proxy for identifying coral symbiosis in the past, particularly when multiple species of corals coexisted in the same environments.
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Symbiosis maintenance in the facultative coral, Oculina arbuscula, relies on nitrogen cycling, cell cycle modulation, and immunity
Abstract 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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- Award ID(s):
- 1937650
- PAR ID:
- 10316721
- Date Published:
- Journal Name:
- Scientific Reports
- Volume:
- 11
- Issue:
- 1
- ISSN:
- 2045-2322
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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.more » « less
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Abstract 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.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1038/s41598-021-00697-6
