An official website of the United States government
Abstract Tropical corals construct the three-dimensional framework for one of the most diverse ecosystems on the planet, providing habitat to a plethora of species across taxa. However, these ecosystem engineers are facing unprecedented challenges, such as increasing disease prevalence and marine heatwaves associated with anthropogenic global change. As a result, major declines in coral cover and health are being observed across the world's oceans, often due to the breakdown of coral-associated symbioses. Here, we review the interactions between the major symbiotic partners of the coral holobiont—the cnidarian host, algae in the family Symbiodiniaceae, and the microbiome—that influence trait variation, including the molecular mechanisms that underlie symbiosis and the resulting physiological benefits of different microbial partnerships. In doing so, we highlight the current framework for the formation and maintenance of cnidarian–Symbiodiniaceae symbiosis, and the role that immunity pathways play in this relationship. We emphasize that understanding these complex interactions is challenging when you consider the vast genetic variation of the cnidarian host and algal symbiont, as well as their highly diverse microbiome, which is also an important player in coral holobiont health. Given the complex interactions between and among symbiotic partners, we propose several research directions and approaches focused on symbiosis model systems and emerging technologies that will broaden our understanding of how these partner interactions may facilitate the prediction of coral holobiont phenotype, especially under rapid environmental change.
more »
« less
Climate Change Leads to a Reduction in Symbiotic Derived Cnidarian Biodiversity on Coral Reefs
Symbiotic relationships enable partners to thrive and survive in habitats where they would either not be as successful, or potentially not exist, without the symbiosis. The coral reef ecosystem, and its immense biodiversity, relies on the symbioses between cnidarians (e.g., scleractinian corals, octocorals, sea anemones, jellyfish) and multiple organisms including dinoflagellate algae (family Symbiodiniaceae), bivalves, crabs, shrimps, and fishes. In this review, we discuss the ramifications of whether coral reef cnidarian symbioses are obligatory, whereby at least one of the partners must be in the symbiosis in order to survive or are facultative. Furthermore, we cover the consequences of cnidarian symbioses exhibiting partner flexibility or fidelity. Fidelity, where a symbiotic partner can only engage in symbiosis with a subset of partners, may be absolute or context dependent. Current literature demonstrates that many cnidarian symbioses are highly obligative and appear to exhibit absolute fidelity. Consequently, for many coral reef cnidarian symbioses, surviving changing environmental conditions will depend on the robustness and potential plasticity of the existing host-symbiont(s) combination. If environmental conditions detrimentally affect even one component of this symbiotic consortium, it may lead to a cascade effect and the collapse of the entire symbiosis. Symbiosis is at the heart of the coral reef ecosystem, its existence, and its high biodiversity. Climate change may cause the demise of some of the cnidarian symbioses, leading to subsequent reduction in biodiversity on coral reefs.
more »
« less
- Award ID(s):
- 1839775
- PAR ID:
- 10226300
- Date Published:
- Journal Name:
- Frontiers in Ecology and Evolution
- Volume:
- 9
- ISSN:
- 2296-701X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Functional genomics is a powerful approach for uncovering molecular mechanisms underlying complex biological processes by linking genetic changes to observable phenotypes. In the context of algal symbiosis, this framework offers significant potential for advancing our understanding of the molecular interactions between marine dinoflagellates and their cnidarian hosts, such as corals—organisms that are foundational to marine ecosystems and biodiversity. As coral bleaching and reef degradation intensify due to environmental stressors, novel strategies are urgently needed to enhance the resilience of these symbiotic partnerships. This opinion piece explores emerging directions in functional genomics as applied to coral–algal symbiosis, with a focus on uncovering the molecular pathways that govern photosynthesis and stress tolerance. We discuss the challenges and opportunities in applying functional genomics to support coral health, improve ecosystem resilience, and inform biotechnological applications in agriculture and medicine. Together, these insights posit the potential for engineered symbioses as a needed focus in mitigating biodiversity loss and supporting sustainable ecosystem management in the face of accelerating environmental change.more » « less
-
ABSTRACT The juxtaposition of highly productive coral reef ecosystems in oligotrophic waters has spurred substantial interest and progress in our understanding of macronutrient uptake, exchange, and recycling among coral holobiont partners (host coral, dinoflagellate endosymbiont, endolithic algae, fungi, viruses, bacterial communities). By contrast, the contribution of trace metals to the physiological performance of the coral holobiont and, in turn, the functional ecology of reef‐building corals remains unclear. The coral holobiont's trace metal economy is a network of supply, demand, and exchanges upheld by cross‐kingdom symbiotic partnerships. Each partner has unique trace metal requirements that are central to their biochemical functions and the metabolic stability of the holobiont. Organismal homeostasis and the exchanges among partners determine the ability of the coral holobiont to adjust to fluctuating trace metal supplies in heterogeneous reef environments. This review details the requirements for trace metals in core biological processes and describes how metal exchanges among holobiont partners are key to sustaining complex nutritional symbioses in oligotrophic environments. Specifically, we discuss how trace metals contribute to partner compatibility, ability to cope with stress, and thereby to organismal fitness and distribution. Beyond holobiont trace metal cycling, we outline how the dynamic nature of the availability of environmental trace metal supplies can be influenced by a variability of abiotic factors (e.g. temperature, light, pH, etc.). Climate change will have profound consequences on the availability of trace metals and further intensify the myriad stressors that influence coral survival. Lastly, we suggest future research directions necessary for understanding the impacts of trace metals on the coral holobiont symbioses spanning subcellular to organismal levels, which will inform nutrient cycling in coral ecosystems more broadly. Collectively, this cross‐scale elucidation of the role of trace metals for the coral holobiont will allow us to improve forecasts of future coral reef function.more » « less
-
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.more » « less
-
Plant–microbe symbioses such as the legume–rhizobium mutualism are vital in the web of ecological relationships within both natural and managed ecosystems, influencing primary productivity, crop yield, and ecosystem services. The outcome of these interactions for plant hosts varies quantitatively and can range from highly beneficial to even detrimental depending on natural genetic variation in microbial symbionts. Here, we take a systems genetics approach, harnessing the genetic diversity present in wild rhizobial populations to predict genes and molecular pathways crucial in determining partner quality, i.e., the benefits of symbiosis for legume hosts. We combine traits, dual-RNAseq of both partners from active nodules, pangenomics/pantranscriptomics, and Weighted Gene Co-expression Network Analysis (WGCNA) for a panel of 20Sinorhizobium melilotistrains that vary in symbiotic partner quality. We find that genetic variation in the nodule transcriptome predicts host plant biomass, and WGCNA reveals networks of genes in plants and rhizobia that are coexpressed and associated with high-quality symbiosis. Presence–absence variation of gene clusters on the symbiosis plasmid (pSymA), validated in planta, is associated with high or low-quality symbiosis and is found within important coexpression modules. Functionally our results point to management of oxidative stress, amino acid and carbohydrate transport, and NCR peptide signaling mechanisms in driving symbiotic outcomes. Our integrative approach highlights the complex genetic architecture of microbial partner quality and raises hypotheses about the genetic mechanisms and evolutionary dynamics of symbiosis.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3389/fevo.2021.636279
