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.

Help Me, Symbionts, You’re My Only Hope: Approaches to Accelerate Our Understanding of Coral Holobiont Interactions

“…Aposymbiotic branches of the facultative coral Oculina arbuscula also exhibit enrichment of gene pathways involved in NF-κB immunity and the inflammatory response compared to symbiotic branches of the same genetic background (Rivera & Davies, 2021). Further, fieldcollected Acropora palmata exhibited upregulation of NF-κB under short-term thermal stress (DeSalvo et al, 2010).…”

“…The answer most likely lies in nutritional benefits provided to the host by the symbiont under ambient conditions. After establishment of symbiosis, the host exerts control over Symbiodiniaceae cell density and proliferation through regulation of the cell cycle and nitrogen cycling (Gorman et al, 2022;Rivera & Davies, 2021).…”

“…The use of A. poculata as an experimental model may allow for better assessment of the role of each symbiotic partner in coral stress responses (i.e., (Wuitchik et al 2021;Sharp et al 2017;Burmester et al 2017;Burmester et al 2018;Holcomb et al 2012), especially because of the importance of symbiosis in coral skeletal growth rate (Chalker and Taylor 1975). In addition to A. poculata, several other reef building species are emerging as potential models, including Oculina arbuscula (Rivera and Davies 2021) and Galaxea fascicularis (Puntin et al 2022), which can both have their symbiotic states experimentally manipulated.…”

Help Me, Symbionts, You’re My Only Hope: Approaches to Accelerate Our Understanding of Coral Holobiont Interactions

“…NF-κB is downregulated following establishment of homologous symbionts in adult and larval Aiptasia compared to aposymbiotic larvae and adults (Wolfowicz et al 2016;Mansfield et al 2017). Aposymbiotic branches of the facultative coral Oculina arbuscula also exhibit enrichment of gene pathways involved in NF-κB immunity compared to symbiotic branches (Rivera and Davies 2021). Further, field-collected Acropora palmata exhibited upregulation of NF-κB transcription under shortterm thermal stress (DeSalvo et al 2010).…”

Editorial: Physiological Regulation and Homeostasis Among Coral Holobiont Partners

“…Environmental nutrients may also be important for the symbiodiniacean dinoflagellates to withstand heat stress ( Zhou et al, 2021 ; Kirk et al Nat Comm), but on the contrary nutrient overloading (eutrophication), particularly in combination with heat stress, can adversely impact the symbiosis and cause bleaching ( D’Angelo and Wiedenmann, 2014 ; Lam et al, 2015 ; Humanes et al, 2016 ; Decarlo et al, 2020 ; Donovan et al, 2020 ). In addition, symbiont cell cycle modulation and host immunity are also critical for the maintenance of the symbiosis ( Rivera and Davies, 2021 ).…”