Host under epigenetic control: A novel perspective on the interaction between microorganisms and corals

Barno, Adam; Villela, Helena; Aranda, Manuel; Thomas, Torsten; Peixoto, Raquel S.

doi:10.1002/bies.202100068

Cited by 20 publications

(21 citation statements)

References 81 publications

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“…Coral reefs have been increasingly challenged by the rate and severity of global change and the inability of their foundational species, reef-building coral, to cope with detrimental effects [112][113][114] . Microbiome-based interventions are promising because they could act on short timescales 115,116 . Desired beneficial roles of coral microbiome members have recently been proposed and summarized 117,118 , together with an experimental framework to identify coral probiotic strains and to reveal mechanisms of action 11,13,117,118 .…”

Section: Coralsmentioning

confidence: 99%

Harnessing the microbiome to prevent global biodiversity loss

et al. 2022

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Global biodiversity loss and mass extinction of species are two of the most critical environmental issues the world is currently facing, resulting in the disruption of various ecosystems central to environmental functions and human health. Microbiome-targeted interventions, such as probiotics and microbiome transplants, are emerging as potential options to reverse deterioration of biodiversity and increase the resilience of wildlife and ecosystems. However, the implementation of these interventions is urgently needed. We summarize the current concepts, bottlenecks and ethical aspects encompassing the careful and responsible management of ecosystem resources using the microbiome (termed microbiome stewardship) to rehabilitate organisms and ecosystem functions. We propose a real-world application framework to guide environmental and wildlife probiotic applications. This framework details steps that must be taken in the upscaling process while weighing risks against the high toll of inaction. In doing so, we draw parallels with other aspects of contemporary science moving swiftly in the face of urgent global challenges.

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Section: Coralsmentioning

confidence: 99%

Harnessing the microbiome to prevent global biodiversity loss

et al. 2022

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“…Through chemical signals and metabolites, endosymbionts can influence epigenomes of host cells and directly enable communication between the two partners 18, 40 . Interestingly, histone acetylase and deacetylase activity have been shown to be influenced by microbes and dietary factors 15, 41, 42 . Although epigenetic studies in cnidarians remain scarce, there is evidence that histone modifications may play a critical role in host-algae symbiosis mechanisms 6, 43, 74, 75 .…”

Section: Discussionmentioning

confidence: 99%

“…Interestingly, histone acetylase and deacetylase activity have been shown to be influenced by microbes and dietary factors 15,41,42 . Although epigenetic studies in cnidarians remain scarce, there is evidence that histone modifications may play a critical role in host-algae symbiosis mechanisms 6,43,74,75 .…”

Section: Discussionmentioning

confidence: 99%

“…However, there are still substantial knowledge gaps in our understanding of the molecular underpinnings of these relationships, especially pertaining to the role of epigenetic mechanisms in regulating the interactions between the host and the symbionts, which remain elusive in cnidarian symbiosis research 6 . The uptake and maintenance of symbionts require specific host responses, such as the suppression of the immune system 7,8,10,15 and the regulation of nutrient fluxes to control symbiont proliferation 9 , to maintain a stable symbiotic relationship. Such responses are mediated through transcriptional changes that are known to be regulated via epigenetic mechanisms in other organisms [10][11][12][13][14] , and some endosymbionts have even been shown to evoke such responses by directly modifying the epigenome of their hosts 10,15 .…”

Section: Introductionmentioning

confidence: 99%

“…The uptake and maintenance of symbionts require specific host responses, such as the suppression of the immune system 7,8,10,15 and the regulation of nutrient fluxes to control symbiont proliferation 9 , to maintain a stable symbiotic relationship. Such responses are mediated through transcriptional changes that are known to be regulated via epigenetic mechanisms in other organisms [10][11][12][13][14] , and some endosymbionts have even been shown to evoke such responses by directly modifying the epigenome of their hosts 10,15 . However, while many recent studies have highlighted the importance of epigenetic mechanisms in maintaining symbiotic relationships in plants and animals [16][17][18] , only one study looking at the role of DNA methylation in symbiosis has been conducted in zooxanthellate cnidarians 6 .…”

Section: Introductionmentioning

confidence: 99%

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Histone modifications and DNA methylation act cooperatively in regulating symbiosis genes in the sea anemone Aiptasia

Nawaz

Cziesielski

Mariappan

et al. 2022

Preprint

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The symbiotic relationship between cnidarians and dinoflagellates is one of the most widespread endosymbiosis in our oceans and provides the ecological basis of coral-reef ecosystems. Although many studies have been undertaken to unravel the molecular mechanisms underlying these symbioses, we still know little about the epigenetic mechanisms that control the transcriptional responses to symbiosis. Here, we used the model organism Exaiptasia diaphana to study the genome-wide patterns and putative functions of the histone modifications H3K27ac, H3K4me3, H3K9ac, H3K36me3 and H3K27me3 in symbiosis. While we find that their functions are generally conserved, we observed that colocalization of more than one modification and or DNA methylation correlated with significantly higher gene expression, suggesting a cooperative action of histone modifications and DNA methylation in promoting gene expression. Analysis of symbiosis genes revealed that activating histone modifications predominantly associated with symbiosis induced genes involved in glucose metabolism, nitrogen transport, amino acid biosynthesis and organism growth while symbiosis suppressed genes were involved in catabolic processes. Our results provide new insights into the mechanisms of prominent histone modifications and their interaction with DNA methylation in regulating symbiosis in cnidarians.

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Abundance of Oligoflexales bacteria is associated with algal symbiont density, independent of thermal stress in Aiptasia anemones

Aguirre,

Fine,

Kenkel

2023

Ecology and Evolution

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Many multicellular organisms, such as humans, plants, and invertebrates, depend on symbioses with microbes for metabolic cooperation and exchange. Reef‐building corals, an ecologically important order of invertebrates, are particularly vulnerable to environmental stress in part because of their nutritive symbiosis with dinoflagellate algae, and yet also benefit from these and other microbial associations. While coral microbiomes remain difficult to study because of their complexity, the anemone Aiptasia is emerging as a simplified model. Research has demonstrated co‐occurrences between microbiome composition and the abundance and type of algal symbionts in cnidarians. However, whether these patterns are the result of general stress‐induced shifts or depletions of algal‐associated bacteria remains unclear. Our study aimed to distinguish the effect of changes in symbiont density and thermal stress on the microbiome of symbiotic Aiptasia strain CC7 by comparing them with aposymbiotic anemones, depleted of their native symbiont, Symbiodinium linucheae. Our analysis indicated that overall thermal stress had the greatest impact on disrupting the microbiome. We found that three bacterial classes made up most of the relative abundance (60%–85%) in all samples, but the rare microbiome fluctuated between symbiotic states and following thermal stress. We also observed that S. linucheae density correlated with abundance of Oligoflexales, suggesting these bacteria may be primary symbionts of the dinoflagellate algae. The findings of this study help expand knowledge on prospective multipartite symbioses in the cnidarian holobiont and how they respond to environmental disturbance.

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Host under epigenetic control: A novel perspective on the interaction between microorganisms and corals

Cited by 20 publications

References 81 publications

Harnessing the microbiome to prevent global biodiversity loss

Harnessing the microbiome to prevent global biodiversity loss

Histone modifications and DNA methylation act cooperatively in regulating symbiosis genes in the sea anemone Aiptasia

Abundance of Oligoflexales bacteria is associated with algal symbiont density, independent of thermal stress in Aiptasia anemones

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