Harnessing the Power of Model Organisms To Unravel Microbial Functions in the Coral Holobiont

Puntin, Giulia; Sweet, Michael; Fraune, Sebastian; Medina, Mónica; Sharp, Koty; Weis, Virginia M.; Ziegler, Maren

doi:10.1128/mmbr.00053-22

Cited by 30 publications

(28 citation statements)

References 343 publications

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“…The richness of the scleractinian taxon offers a vast array of species to choose from in the quest for a suitable candidate coral model species. These can be evaluated for their tractability (as amenability to experimental work) considering several aspects which, as proposed by Puntin et al (2022), should include: (1) pre-existing knowledge: baseline information of the organism's biology is necessary to interpret and contextualize results; (2) compatibility with aquarium rearing: the possibility to maintain the organism and preferably to complete its life cycle in the laboratory is essential to increase its availability, reduce confounding effects such as unknown life history, improve reproducibility, and lower the pressure on threatened wild populations;…”

Section: Introductionmentioning

confidence: 99%

The reef-building coral Galaxea fascicularis: a new model system for coral symbiosis research

et al. 2022

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Reef-building corals owe their evolutionary success to their symbiosis with unicellular algae (Symbiodiniaceae). However, increasingly frequent heat waves lead to coral mass-bleaching events and pose a serious threat to the survival of reef ecosystems. Despite significant efforts, a mechanistic understanding of coral–algal symbiosis functioning, what leads to its breakdown and what can prevent it, remains incomplete. The main obstacles are low amenability of corals to experimental handling and, owing to its obligatory nature, the difficulties of manipulating the coral–algal association. Indeed, many studies on the symbiotic partnership are conducted on other cnidarian model organisms and their results may therefore not be fully transferable to tropical reef-building corals. Here, we identify the tropical stony coral species Galaxea fascicularis as a novel candidate coral model system. Individual polyps of this species can be separated, enabling highly replicated genotype studies, and are well suited to experimental investigation of the symbiosis as they can be easily and effectively rid of their algal symbionts (bleached). We show that bleached adult individuals can reestablish symbiosis with non-native symbionts, and we report the completion of the gametogenic cycle ex situ, with the successful spawning in aquaria over multiple years. These achievements help overcome several of the major limitations to direct research on corals and highlight the potential of G. fascicularis as an important new model system for investigations of symbiosis functioning and manipulation.

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Section: Introductionmentioning

confidence: 99%

The reef-building coral Galaxea fascicularis: a new model system for coral symbiosis research

et al. 2022

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“…Reef-building corals are assemblages of cnidarian host cells, intracellular photosynthetic algae (Family Symbiodiniaceae) and a complex microbiome [1]. These symbioses enable corals to flourish in nutrient-poor waters [2].…”

Section: Introductionmentioning

confidence: 99%

“…Taken together, two central themes of cnidarian symbiosis emerge: (1) symbiosis modulates host immunity, and (2) heterotrophy modulates symbiosis. However, the influence of symbiosis and nutrition on immunity, and on the individual regulatory pathways of the cnidarian immune system, remains largely unexplored, but may provide insight for understanding cnidarian stress responses.…”

Section: Introductionmentioning

confidence: 99%

Starvation differentially affects gene expression, immunity and pathogen susceptibility across symbiotic states in a model cnidarian

Valadez-Ingersoll,

Aguirre Carrión,

Bodnar

et al. 2024

Proc. R. Soc. B.

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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 anemone Exaiptasia 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.

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“…The richness of the scleractinian taxon offers a vast array of species to choose from in the quest for a suitable candidate coral model species. These can be evaluated for their tractability (as amenability to experimental work) considering several aspects which, as proposed by Puntin et al (2022) should include: 1) pre-existing knowledge: baseline information of the organism’s biology is necessary to interpret and contextualize results; 2) compatibility with aquarium rearing: the possibility to maintain the organism and preferably to complete its life cycle in the lab is essential to increase its availability, reduce confounding effects such as unknown life history, improve reproducibility, and lower the pressure on threatened wild populations; 3) amenability to symbiosis manipulations is necessary to help unravel complex coral-algal functional interactions, and can be broken down into the organism’s suitability to be rendered aposymbiotic (bleached), to be maintained aposymbiotic for a certain time, and to then be re-infected with Symbiodiniaceae.…”

Section: Introductionmentioning

confidence: 99%

The reef-building coralGalaxea fascicularis: a new model system for coral symbiosis research

Puntin

Craggs

Hayden

et al. 2022

Preprint

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Reef-building corals owe their evolutionary success to their symbiosis with unicellular algae (Symbiodiniaceae). However, increasingly frequent heat waves lead to coral mass-bleaching events and pose a serious threat to the survival of reef ecosystems. Despite significant efforts, a mechanistic understanding of coral-algal symbiosis functioning, what leads to its breakdown and what can prevent it, remains incomplete. The main obstacles are low amenability of corals to experimental handling and, owing to its obligatory nature, the difficulties of manipulating the coral-algal association. Indeed, many studies on the symbiotic partnership are conducted on other cnidarian model organisms and their results may therefore not be fully transferable to tropical reef-building corals. Here, we identify the tropical stony coral species Galaxea fascicularis as a novel candidate coral model system. Individual polyps of this species can be separated, enabling highly replicated genotype studies, and are well suited to experimental investigation of the symbiosis as they can be easily and effectively rid of their algal symbionts (bleached). We show that bleached adult individuals can reestablish symbiosis with homologous and heterologous symbionts. We also report the completion of the gametogenic cycle ex-situ and the successful spawning in aquaria over multiple years. These achievements help overcome several of the major limitations to direct research on corals and highlight the potential of G. fascicularis as an important new model system for investigations of symbiosis functioning and manipulation.

show abstract

Harnessing the Power of Model Organisms To Unravel Microbial Functions in the Coral Holobiont

Cited by 30 publications

References 343 publications

The reef-building coral Galaxea fascicularis: a new model system for coral symbiosis research

The reef-building coral Galaxea fascicularis: a new model system for coral symbiosis research

Starvation differentially affects gene expression, immunity and pathogen susceptibility across symbiotic states in a model cnidarian

The reef-building coralGalaxea fascicularis: a new model system for coral symbiosis research

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