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1. Tentacle patterning during Exaiptasia diaphana pedal lacerate development differs between symbiotic and aposymbiotic animals

   https://doi.org/10.7717/peerj.12770  

   Presnell, Jason S.; Wirsching, Elizabeth; Weis, Virginia M. (January 2022, PeerJ)

   Exaiptasia diaphana , a tropical sea anemone known as Aiptasia, is a tractable model system for studying the cellular, physiological, and ecological characteristics of cnidarian-dinoflagellate symbiosis. Aiptasia is widely used as a proxy for coral-algal symbiosis, since both Aiptasia and corals form a symbiosis with members of the family Symbiodiniaceae. Laboratory strains of Aiptasia can be maintained in both the symbiotic (Sym) and aposymbiotic (Apo, without algae) states. Apo Aiptasia allow for the study of the influence of symbiosis on different biological processes and how different environmental conditions impact symbiosis. A key feature of Aiptasia is the ease of propagating both Sym and Apo individuals in the laboratory through a process called pedal laceration. In this form of asexual reproduction, small pieces of tissue rip away from the pedal disc of a polyp, then these lacerates eventually develop tentacles and grow into new polyps. While pedal laceration has been described in the past, details of how tentacles are formed or how symbiotic and nutritional state influence this process are lacking. Here we describe the stages of development in both Sym and Apo pedal lacerates. Our results show that Apo lacerates develop tentacles earlier than Sym lacerates, while over the course of 20 days, Sym lacerates end up with a greater number of tentacles. We describe both tentacle and mesentery patterning during lacerate development and show that they form through a single pattern in early stages regardless of symbiotic state. In later stages of development, Apo lacerate tentacles and mesenteries progress through a single pattern, while variable patterns were observed in Sym lacerates. We discuss how Aiptasia lacerate mesentery and tentacle patterning differs from oral disc regeneration and how these patterning events compare to postembryonic development in Nematostella vectensis , another widely-used sea anemone model. In addition, we demonstrate that Apo lacerates supplemented with a putative nutrient source developed an intermediate number of tentacles between un-fed Apo and Sym lacerates. Based on these observations, we hypothesize that pedal lacerates progress through two different, putatively nutrient-dependent phases of development. In the early phase, the lacerate, regardless of symbiotic state, preferentially uses or relies on nutrients carried over from the adult polyp. These resources are sufficient for lacerates to develop into a functional polyp. In the late phase of development, continued growth and tentacle formation is supported by nutrients obtained from either symbionts and/or the environment through heterotrophic feeding. Finally, we advocate for the implementation of pedal lacerates as an additional resource in the Aiptasia model system toolkit for studies of cnidarian-dinoflagellate symbiosis. 

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

   https://doi.org/10.1098/rspb.2023.1685  

   Valadez-Ingersoll, Maria; Aguirre Carrión, Pablo J.; Bodnar, Caoimhe A.; Desai, Niharika A.; Gilmore, Thomas D.; Davies, Sarah W. (February 2024, Proceedings of the Royal Society B: Biological Sciences)

   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. 

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3. Systematic review of cnidarian microbiomes reveals insights into the structure, specificity, and fidelity of marine associations

   https://doi.org/10.1038/s41467-023-39876-6  

   McCauley, M; Goulet, T L; Jackson, C R; Loesgen, S (December 2023, Nature Communications)

   Abstract Microorganisms play essential roles in the health and resilience of cnidarians. Understanding the factors influencing cnidarian microbiomes requires cross study comparisons, yet the plethora of protocols used hampers dataset integration. We unify 16S rRNA gene sequences from cnidarian microbiome studies under a single analysis pipeline. We reprocess 12,010 cnidarian microbiome samples from 186 studies, alongside 3,388 poriferan, 370 seawater samples, and 245 cultured Symbiodiniaceae, unifying ~6.5 billion sequence reads. Samples are partitioned by hypervariable region and sequencing platform to reduce sequencing variability. This systematic review uncovers an incredible diversity of 86 archaeal and bacterial phyla associated with Cnidaria, and highlights key bacteria hosted across host sub-phylum, depth, and microhabitat. Shallow (< 30 m) water Alcyonacea and Actinaria are characterized by highly shared and relatively abundant microbial communities, unlike Scleractinia and most deeper cnidarians. Utilizing the V4 region, we find that cnidarian microbial composition, richness, diversity, and structure are primarily influenced by host phylogeny, sampling depth, and ocean body, followed by microhabitat and sampling date. We identify host and geographical generalist and specificEndozoicomonasclades within Cnidaria and Porifera. This systematic review forms a framework for understanding factors governing cnidarian microbiomes and creates a baseline for assessing stress associated dysbiosis. 

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4. Comparative physiology reveals heat stress disrupts acid–base homeostasis independent of symbiotic state in the model cnidarian Exaiptasia diaphana

   https://doi.org/10.1242/jeb.246222  

   Allen-Waller, Luella R.; Jones, Katelyn G.; Martynek, Marcelina P.; Brown, Kristen T.; Barott, Katie L. (February 2024, Journal of Experimental Biology)

   Climate change threatens the survival of symbiotic cnidarians by causing photosymbiosis breakdown in a process known as bleaching. Direct effects of temperature on cnidarian host physiology remain difficult to describe because heatwaves depress symbiont performance, leading to host stress and starvation. The symbiotic sea anemone Exaiptasia diaphana provides an opportune system to disentangle direct versus indirect heat effects on the host, as it can survive indefinitely without symbionts. We tested the hypothesis that heat directly impairs cnidarian physiology by comparing symbiotic and aposymbiotic individuals of two laboratory subpopulations of a commonly used clonal strain of E. diaphana, CC7. We exposed anemones to a range of temperatures (ambient, +2°C, +4°C and +6°C) for 15–18 days, then measured their symbiont population densities, autotrophic carbon assimilation and translocation, photosynthesis, respiration and host intracellular pH (pHi). Symbiotic anemones from the two subpopulations differed in size and symbiont density and exhibited distinct heat stress responses, highlighting the importance of acclimation to different laboratory conditions. Specifically, the cohort with higher initial symbiont densities experienced dose-dependent symbiont loss with increasing temperature and a corresponding decline in host photosynthate accumulation. In contrast, the cohort with lower initial symbiont densities did not lose symbionts or assimilate less photosynthate when heated, similar to the response of aposymbiotic anemones. However, anemone pHi decreased at higher temperatures regardless of cohort, symbiont presence or photosynthate translocation, indicating that heat consistently disrupts cnidarian acid–base homeostasis independent of symbiotic status or mutualism breakdown. Thus, pH regulation may be a critical vulnerability for cnidarians in a changing climate. 

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5. Microbiome depletion and recovery in the sea anemone, Exaiptasia diaphana , following antibiotic exposure

   https://doi.org/10.1128/msystems.01342-23  

   MacVittie, Sophie; Doroodian, Saam; Alberto, Aaron; Sogin, Maggie (May 2024, mSystems)

   Wilkins, Laetitia_G E (Ed.)

   ABSTRACT Microbial species that comprise host-associated microbiomes play an essential role in maintaining and mediating the health of plants and animals. While defining the role of individual or even complex communities is important toward quantifying the effect of the microbiome on host health, it is often challenging to develop causal studies that link microbial populations to changes in host fitness. Here, we investigated the impacts of reduced microbial load following antibiotic exposure on the fitness of the anemone,Exaiptasia diaphanaand subsequent recovery of the host’s microbiome. Anemones were exposed to two different types of antibiotic solutions for 3 weeks and subsequently held in sterilized seawater for a 3-week recovery period. Our results revealed that both antibiotic treatments reduced the overall microbial load during and up to 1 week post-treatment. The observed reduction in microbial load was coupled with reduced anemone biomass, halted asexual reproduction rates, and for one of the antibiotic treatments, the partial removal of the anemone’s algal symbiont. Finally, our amplicon sequencing results of the 16S rRNA gene revealed that anemone bacterial composition only shifted in treated individuals during the recovery phase of the experiment, where we also observed a significant reduction in the overall diversity of the microbial community. Our work implies that theE. diaphana’smicrobiome contributes to host fitness and that the recovery of the host’s microbiome following disturbance with antibiotics leads to a reduced, but stable microbial state.IMPORTANCEExaiptasia diaphanais an emerging model used to define the cellular and molecular mechanisms of coral-algal symbioses.E. diaphanaalso houses a diverse microbiome, consisting of hundreds of microbial partners with undefined function. Here, we applied antibiotics to quantify the impact of microbiome removal on host fitness as well as define trajectories in microbiome recovery following disturbance. We showed that reduction of the microbiome leads to negative impacts on host fitness, and that the microbiome does not recover to its original composition while held under aseptic conditions. Rather the microbiome becomes less diverse, but more consistent across individuals. Our work is important because it suggests that anemone microbiomes play a role in maintaining host fitness, that they are susceptible to disturbance events, and that it is possible to generate gnotobiotic individuals that can be leveraged in microbiome manipulation studies to investigate the role of individual species on host health. 

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