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The upside-down jellyfish holobiont,Cassiopea xamachana, is a useful model system for tri-partite interactions between the cnidarian host, the photosymbiont, and the bacterial microbiome. While the interaction between the host and photosymbiont has been well studied, less is understood of the associated bacterial community. To date, the bacterial microbiome of wildC. xamachanahas remained largely uncharacterized. Thus, wild medusae (n=6) and larvae (n=3) were collected from two sites in the Florida Keys. Bacterial community composition was characterized via amplicon sequencing of the 16S rRNA gene V4 region. The medusa bacterial community was dominated by members of the Alphaproteobacteria and Gammaproteobacteria, while Planctomycetota, Actinomycetota, Bacteroidota, and Bacillota were also present, among others. Community composition was consistent between locations and across medusa structures (oral arm, bell, and gonad). The larval bacterial community clustered apart from the medusa community in beta diversity analysis and was characterized by the presence of several Pseudomonadota taxa that were not present in the medusa, including theAlteromonas,Pseudoalteromonas, andThalassobiusgenera. A bacterial isolate library encompassing much of the amplicon sequencing diversity was also developed and tested via metabolic assays in a separate culture-dependent analysis of isolates from medusa bells, oral arms, and laplets. Most characteristics were not correlated with host sex or medusa structure, but gelatinase production was more common in laplet isolates, while lactose fermentation was more common in female oral arm isolates. TheEndozoicomonasgenus was dominant in both amplicon sequencing and in our isolate library, and was equally prevalent across all medusa structures and in both sexes. Understanding the bacterial component of theC. xamachanaholobiont will allow us to further develop this important model cnidarian holobiont. 

Abstract BackgroundEvolutionary tradeoffs between life-history strategies are important in animal evolution. Because microbes can influence multiple aspects of host physiology, including growth rate and susceptibility to disease or stress, changes in animal-microbial symbioses have the potential to mediate life-history tradeoffs. Scleractinian corals provide a biodiverse, data-rich, and ecologically-relevant host system to explore this idea. ResultsUsing a comparative approach, we tested if coral microbiomes correlate with disease susceptibility across 425 million years of coral evolution by conducting a cross-species coral microbiome survey (the “Global Coral Microbiome Project”) and combining the results with long-term global disease prevalence and coral trait data. Interpreting these data in their phylogenetic context, we show that microbial dominance predicts disease susceptibility, and traced this dominance-disease association to a single putatively beneficial symbiont genus,Endozoicomonas. Endozoicomonasrelative abundance in coral tissue explained 30% of variation in disease susceptibility and 60% of variation in microbiome dominance across 40 coral genera, while also correlating strongly with high growth rates. ConclusionsThese results demonstrate that the evolution ofEndozoicomonassymbiosis in corals correlates with both disease prevalence and growth rate, and suggest a mediating role. Exploration of the mechanistic basis for these findings will be important for our understanding of how microbial symbioses influence animal life-history tradeoffs. 

The regenerative capacity of Scyphozoans (Phylum Cnidaria) has been relatively understudied. The model organism Cas- siopea xamachana hosts photosynthetic dinoflagellate symbionts in the host’s motile amoebocyte cells. A handful of studies have reported regeneration in the polyps of C. xamachana, but the mechanisms underlying regeneration have not been fully explored. Despite undergoing drastic developmental changes when symbiotic, the effect of symbiont presence and species on host regeneration has never been explored. C. xamachana polyps were decapitated when aposymbiotic, and symbiotic with both a homologous and a heterologous symbiont species. Regeneration and asexual budding were observed, and EdU labeling was performed to observe patterns of cell proliferation in regenerating polyps. The presence of symbionts increased likelihood to regenerate, yet symbiont species did not affect success of regeneration. No blastema or dividing cells were observed, implying cell proliferation is not the primary mechanism behind regeneration in polyps of C. xamachana. 

Coral disease has progressively become one of the most pressing issues affecting coral reef survival. In the last 50 years, several reefs throughout the Caribbean have been severely impacted by increased frequency and intensity of disease outbreaks leading to coral death. A recent example of this is stony coral tissue loss disease which has quickly spread throughout the Caribbean, devastating coral reef ecosystems. Emerging from these disease outbreaks has been a coordinated research response that often integrates ‘omics techniques to better understand the coral immune system. ‘Omics techniques encompass a wide range of technologies used to identify large scale gene, DNA, metabolite, and protein expression. In this review, we discuss what is known about coral immunity and coral disease from an ‘omics perspective. We reflect on the development of biomarkers and discuss ways in which coral disease experiments to test immunity can be improved. Lastly, we consider how existing data can be better leveraged to combat future coral disease outbreaks. 

Metazoans host complex communities of microorganisms that include dinoflagellates, fungi, bacteria, archaea and viruses. Interactions among members of these complex assemblages allow hosts to adjust their physiology and metabolism to cope with environmental variation and occupy different habitats. Here, using reciprocal transplantation across depths, we studied adaptive divergence in the corals Orbicella annularis and O. franksi , two young species with contrasting vertical distribution in the Caribbean. When transplanted from deep to shallow, O. franksi experienced fast photoacclimation and low mortality, and maintained a consistent bacterial community. By contrast, O. annularis experienced high mortality and limited photoacclimation when transplanted from shallow to deep. The photophysiological collapse of O. annularis in the deep environment was associated with an increased microbiome variability and reduction of some bacterial taxa. Differences in the symbiotic algal community were more pronounced between coral species than between depths. Our study suggests that these sibling species are adapted to distinctive light environments partially driven by the algae photoacclimation capacity and the microbiome robustness, highlighting the importance of niche specialization in symbiotic corals for the maintenance of species diversity. Our findings have implications for the management of these threatened Caribbean corals and the effectiveness of coral reef restoration efforts. 

Coevolution—reciprocal evolutionary change between interacting lineages (Thompson, 1994; see Glossary)—is thought to have played a profound role in the evolution of Life on Earth. From similar patterns across the wings of unrelated lineages of butterflies (Hoyal Cuthill and Charleston, 2015), egg mimicry of “cheating” brood parasites (Davies, 2010), to the role of animal pollinators in driving the diversification of flowering plants (Kay and Sargent, 2009), to the ubiquity of sexual reproduction and sexual conflicts (Hamilton, 2002; Arnqvist and Rowe, 2005; King et al., 2009), the formation of the eukaryotic cell (Martin et al., 2015; Imachi et al., 2020), and even the origin of living organisms themselves (Mizuuchi and Ichihashi, 2018), evolutionary changes among interacting lineages have played profound and important roles in the history of Life. This Grand Challenges inaugural contribution encompasses eclectic opinions of the editorial board as to what are the next frontiers of coevolution research in the 21st century. Coevolutionary biology is a field that has garnered a lot of attention in recent years, in part as a result of technical advances in nucleotide sequencing and bioinformatics in the burgeoning field of host–microbial interactions. Many seminal studies of coevolution examined reciprocal evolutionary change between two or a few interacting macroscopic species that imposed selective pressures on one another (e.g., insect or bird pollinators and their flowering host plants). Understanding the contexts under which coevolution occurs, as opposed to scenarios in which each partner adapts independently to a particular environment (Darwin, 1862; Stiles, 1978) is important to elucidate coevolutionary processes. A whole spectrum of organismal interactions has been examined under the lens of coevolution, providing additional context, and nuance to ecological strategies traditionally categorized as ranging from beneficial to detrimental for participating species (Figure 1). In particular, a coevolutionary perspective has revealed that even “mutualisms” are not always fully beneficial or cooperative for the partners involved. Instead, the tendency to “cheat” permeates across symbiotic partnerships (Perez-Lamarque et al., 2020). Conversely, recent evidence suggests that non-lethal predation by co-evolved predators, which has traditionally been assumed to be entirely antagonistic, may provide sessile prey with some indirect benefit through enhanced opportunities to acquire beneficial symbiotic microorganisms (Grupstra et al., 2021). Herein, we discuss some of the recent areas of active research in coevolution, restricting our focus to coevolution between interacting species. 

Coral reefs are declining worldwide primarily because of bleaching and subsequent mortality resulting from thermal stress. Currently, extensive efforts to engage in more holistic research and restoration endeavors have considerably expanded the techniques applied to examine coral samples. Despite such advances, coral bleaching and restoration studies are often conducted within a specific disciplinary focus, where specimens are collected, preserved, and archived in ways that are not always conducive to further downstream analyses by specialists in other disciplines. This approach may prevent the full utilization of unexpended specimens, leading to siloed research, duplicative efforts, unnecessary loss of additional corals to research endeavors, and overall increased costs. A recent US National Science Foundation-sponsored workshop set out to consolidate our collective knowledge across the disciplines of Omics, Physiology, and Microscopy and Imaging regarding the methods used for coral sample collection, preservation, and archiving. Here, we highlight knowledge gaps and propose some simple steps for collecting, preserving, and archiving coral-bleaching specimens that can increase the impact of individual coral bleaching and restoration studies, as well as foster additional analyses and future discoveries through collaboration. Rapid freezing of samples in liquid nitrogen or placing at −80 °C to −20 °C is optimal for most Omics and Physiology studies with a few exceptions; however, freezing samples removes the potential for many Microscopy and Imaging-based analyses due to the alteration of tissue integrity during freezing. For Microscopy and Imaging, samples are best stored in aldehydes. The use of sterile gloves and receptacles during collection supports the downstream analysis of host-associated bacterial and viral communities which are particularly germane to disease and restoration efforts. Across all disciplines, the use of aseptic techniques during collection, preservation, and archiving maximizes the research potential of coral specimens and allows for the greatest number of possible downstream analyses.