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As coral reefs struggle to survive under climate change, it is crucial to know whether they have the capacity to withstand changing conditions, particularly increasing seawater temperatures. Thermal tolerance requires the integrative response of the different components of the coral holobiont (coral host, algal photosymbiont, and associated microbiome). Here, using a controlled thermal stress experiment across three divergent Caribbean coral species, we attempt to dissect holobiont member metatranscriptome responses from coral taxa with different sensitivities to heat stress and use phylogenetic ANOVA to study the evolution of gene expression adaptation. We show that coral response to heat stress is a complex trait derived from multiple interactions among holobiont members. We identify host and photosymbiont genes that exhibit lineage-specific expression level adaptation and uncover potential roles for bacterial associates in supplementing the metabolic needs of the coral-photosymbiont duo during heat stress. Our results stress the importance of integrative and comparative approaches across a wide range of species to better understand coral survival under the predicted rise in sea surface temperatures. As corals struggle to survive under climate change, it is crucial to know whether they can withstand increasing seawater temperatures. Using a controlled thermal stress experiment across three divergent coral holobionts, this study examines metatranscriptomic responses to heat stress corresponding to the coral host, photosymbionts and associated microbiota.

In this study, we explore how the Caribbean coral  Orbicella faveolata  recovers after bleaching, using fragments from 13 coral colonies exposed to heat stress (32 °C) for ten days. Biological parameters and coral optical properties were monitored during and after the stress. Increases in both, the excitation pressure over photosystem II ( Qm ) and pigment specific absorption (a* Chl a ) were observed in the stressed corals, associated with reductions in light absorption at the chlorophyll  a  red peak ( D e675 ) and symbiont population density. All coral fragments exposed to heat stress bleached but a fraction of the stressed corals recovered after removing the stress, as indicated by the reductions in  Q m  and increases in  D e675  and the symbiont population observed. This subsample of the experimentally bleached corals also showed blooms of the endolithic algae  Ostreobium  spp. underneath the tissue. Using a numerical model, we quantified the amount of incident light reflected by the coral, and absorbed by the different pigmented components: symbionts, host-tissue and  Ostreobium spp. Our study supports the key contribution of  Ostreobium spp .  blooms near the skeletal surface, to coral recovery after bleaching by reducing skeleton reflectance. Endolithic blooms can thus significantly alleviate the high light stress that affects the remaining symbionts during the stress or when the coral has achieved the bleached phenotype.

Invasive marine parasites can be established long before their introduction mechanisms are resolved, and factors contributing to their successes are often unknown. Understanding the ecology of these invasive parasites is urgently needed for economic and resource conservation efforts. In the eastern Pacific, the introduced Asian bopyid parasite, Orthione griffenis, extends at least from Sitka, Alaska, USA to San Quintín, Baja California, Mexico. In the new range, it infests at least two native hosts and one introduced host. We examined the genetic structure of O. griffenis from Morro Bay, California, to Ketchikan, Alaska, based on Double digest restriction‐site associated DNA (ddRAD) sequencing, and estimated its larval dispersal range from laboratory‐based survival tests. There was a lack of genetic diversity, structure, and isolation by distance across O. griffenis populations. There was also a lower‐than‐expected genetic polymorphism, consistent with previous hypotheses of its dispersal away from a single colonization event by a small number of initial propagules. Orthione griffenis larval survival appears sufficient for dispersal in coastal ocean currents over the observed northern invasion range and for transpacific dispersal via ballast water. The natural history and interaction of O. griffenis with its new and original hosts provide a unique system for understanding species adaptation in invaded ecosystems. This work demonstrates how genetically homogeneous invasive parasite populations can rapidly expand and potentially alter marine communities. Expanded efforts to understand the interactions of parasites and their vectors in their native and non‐indigenous habitats are critically needed for detecting, limiting, and mitigating their effects on endemic marine communities. This study examined the genetic structure of the invasive isopod parasite, Orthione griffenis, between Morro Bay, California, and Ketchikan, Alaska, using ddRAD sequencing and estimated its larval dispersal range from laboratory‐based survival tests. There was a lack of genetic diversity, structure, and isolation by distance across O. griffenis populations. This work highlights the potential for genetically homogeneous invasive parasite populations to rapidly expand and force fundamental alterations of marine communities.

Photosymbioses between Cnidarians and algae are widespread in marine ecosystems. The jellyfish Cassiopea - Symbiodinium symbiosis serves as a valuable model for studying host-symbiont interactions in photosymbiotic organisms. Despite its ecological similarity to coral symbiosis, the effects of rising sea surface temperatures on Cassiopea symbiosis, particularly during early developmental stages, remain unexplored. By exposing Symbiodinium cultures to heat stress and subsequently using these symbionts to colonize jellyfish polyps under ambient and elevated temperature conditions, we study the impact of heat on microbe-stimulating strobilation. We observed a significant reduction in chlorophyll concentration in heat-stressed Symbiodinium algae. Polyps colonized with these symbionts exhibited delayed strobilation under ambient conditions and failed to undergo strobilation under continued heat stress. Additionally, we found abnormal ephyra morphology and increased rates of asexual reproduction under heat stress. Our findings suggest that ocean warming may disrupt critical stages of Cassiopea strobilation and development, ultimately threatening their population stability under warming marine environments.

Animals often acquire their microbial symbionts from the environment, but the mechanisms underlying how specificity of the association is achieved are poorly understood. We demonstrate that the conserved proton pump, V-type ATPase (VHA), plays a key role in the establishment of the model light-organ symbiosis between the squid Euprymna scolopes and its bacterial partner, Vibrio fischeri . Recruitment of V. fischeri from the surrounding seawater is mediated by juvenile-specific ciliated fields on the organ’s surface. These epithelia produce acidic mucus containing antimicrobials with low-pH optima, creating a chemical environment fostering specific recruitment of V. fischeri . We provide evidence that this critical acidic landscape is created by activity of VHA. VHA inhibition abolished epithelial-cell acidity, resulting in increased mucus pH and inefficient symbiont colonization. Thus, VHA provides a mechanistic link between host modulation of microenvironmental acidity, immune function, and selection of microbial symbionts, a strategy for specificity that may govern other symbioses. Production of an acidic microenvironment by the juvenile host’s epithelial V-type ATPase promotes the recruitment of its specific bacterial symbiont from the ambient environment.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Photosymbioses between Cnidarians and algae are widespread in marine ecosystems. The jellyfish Cassiopea-Symbiodinium symbiosis serves as a valuable model for studying host-symbiont interactions in photosymbiotic organisms. Despite its ecological similarity to coral symbiosis, the effects of rising sea surface temperatures on Cassiopea symbiosis, particularly during early developmental stages, remain unexplored. By exposing Symbiodinium cultures to heat stress and subsequently using these symbionts to colonize jellyfish polyps under ambient and elevated temperature conditions, we study the impact of heat on microbe-stimulating metamorphosis. We observed a significant reduction in chlorophyll concentration in heat-stressed Symbiodinium algae. Polyps colonized with these symbionts exhibited delayed metamorphosis under ambient conditions and failed to undergo metamorphosis under continued heat stress. Additionally, we found abnormal ephyra morphology and increased rates of asexual reproduction under heat stress. Our findings suggest that ocean warming may disrupt critical stages of Cassiopea metamorphosis and development by impairing symbiosis, ultimately threatening their population stability under warming marine environments.

Cnidaria forms many kinds of symbiosis, one that has been extremely successful is that of the scleractinian – Symbiodiniaceae photosymbiosis. This intimate interaction creates a habitat for a diverse community of bacteria, archaea, eukaryotes, and viruses – together they form the coral holobiont. Earlier studies show that elevated seawater temperatures cause dissociation of component taxa and lead to the breakdown of the holobiont. The breakdown process starts with the disassociation between the Symbiodiniaceae and the host, subsequently causing coral bleaching. Bleaching leads to shifts in the associated microbial communities giving rise to complete dysbiosis. To date, neither the dynamics of the constituent taxa during the breakdown process nor the underlying molecular basis, have been systematically studied in a comparative framework. Metatranscriptomic approaches provide an immense resource to examine multipartite interactions within the coral holobiont and their response to varying environmental conditions. In Chapter 2, I studied the effects of heat stress in the three Caribbean coral species Orbicella faveolata, Pseudodiploria clivosa, and Sidersastrea radians. I described the metabolic contribution of coral host, Symbiodiniaceae, and other microbiota to holobiont function in response to elevated temperature. I found functional evidence that coexistent coral holobiont associates display different responses and metabolic capabilities under elevated temperature stress. Resistance observed in robust coral holobionts may be explained in part by the redundancy of key metabolic pathways from different holobiont members.Elevated temperatures as a consequence of global change pose a threat for coral species, but adaptive evolution could guarantee the persistence of species. In chapter 3, by using a phylogenetic framework, I examined the evolution of gene expression on the three aforementioned species and their Symbiodiniaceae photosymbionts. I uncovered genes that have maintained conserved expression over evolutionary time and others that may have undergone expression level adaptation pertinent to heat stress. My analyses reveal host gene candidates with a potential adaptive expression involved in key metabolic functions such as protein processing, ER to Golgi vesiclemediated transport, ubiquitination, fatty acid biosynthesis, metabolism of cofactors and vitamins, cell redox homeostasis, transport, autophagosome maturation, mRNA splicing, DNA repair, apoptosis, and the carbon concentration mechanism. Gene candidates from the symbiont with a divergent expression between lineages are related to lipid catabolism, ubiquitination, cell division and proliferation, chlorophyll biosynthesis, cell redox homeostasis and protein processing and folding. The evolution of gene expression levels reflects the lineage-specific adaptations across both host and symbiont phylogeny.In chapter 4, I tried to understand the transcriptional and post-transcriptional regulation of gene expression via miRNAs during symbiosis and metamorphosis of symbiotic cnidarian, Cassiopea xamachana, an emerging model system for cnidarian algal photosymbiosis. By infecting hosts with either a homologous or heterologous Symbiodinium spp. we established a comparative framework to assess if there is a conservation in miRNA regulatory networks involved in regulation of symbiosis. Through small RNA and transcriptomic profiling, we identified miRNAs in C. xamachana expressed during the onset of symbiosis and metamorphosis stages and during symbiosis breakdown under thermal stress in fully developed/symbiotic strobilae. My results suggest that the ability of miRNAs to fine-tune gene expression, enabling different levels of interaction between host and a wide range of symbionts without risking absolute incompatibility. Taken all together, these findings demonstrate the importance of a comparative genomics approach to dissect the complex responses of organisms living in symbiosis, as well as the evolution of the expression as a result of the holobiont member interactions during heat stress and developmental stages. Due to the complexity of cnidarian-algal photosymbiosis and the involvement of multiple layers of interactions across kingdoms, it is difficult to generalize the findings of a limited number of model systems to a full understanding of this important biological system. Therefore, this work paves the way for a comparative genomics framework that is grounded in phylogenetic inference to examine the evolutionary trajectories of the molecular basis of such complex interactions in a wider range of cnidarian-algal species. While the examination of heat stress is particularly of most interest to the current adversity faced by coral reefs worldwide due to anthropogenic impact and climate change, insights gained in this thesis about potential regulatory mechanisms such as metabolic control and miRNAs controlling the robustness of the holobiont and their role in symbiont compatibility leaves many questions open for future research.

Microbes can initiate developmental gene regulatory cascade in animals. The molecular mechanisms underlying microbe-induced animal development and the evolutionary steps to integrate microbial signals into regulatory programs remain poorly understood. In the upside-down jellyfish Cassiopea xamachana, a dinoflagellate endosymbiont initiates the life stage transition from the sessile polyp to the sexual medusa. We found that metabolic products derived from symbiont carotenoids are important to initiate C. xamachana development in addition to conserved genes involved in medusa development of non-symbiotic jellyfish. We also revealed transcription factor COUP as a co-regulator of nuclear receptor RXR during metamorphosis. These data suggest relatively few steps may be necessary to integrate symbiont signals into gene regulatory networks and cements the role of the symbiont as a key trigger for life history transition in C. xamachana. Competing Interest Statement The authors have declared no competing interest.