The coral microbiome: towards an understanding of the molecular mechanisms of coral–microbiota interactions

FEMS Microbiology Reviews, Journal Year: 2023, Volume and Issue: 47(2)

Published: March 1, 2023

Corals live in a complex, multipartite symbiosis with diverse microbes across kingdoms, some of which are implicated vital functions, such as those related to resilience against climate change. However, knowledge gaps and technical challenges limit our understanding the nature functional significance complex symbiotic relationships within corals. Here, we provide an overview complexity coral microbiome focusing on taxonomic diversity functions well-studied cryptic microbes. Mining literature indicate that while corals collectively harbour third all marine bacterial phyla, known symbionts antagonists represent minute fraction this these taxa cluster into select genera, suggesting selective evolutionary mechanisms enabled bacteria gain niche holobiont. Recent advances research aimed at leveraging manipulation increase coral's fitness help mitigate heat stress-related mortality discussed. Then, insights potential through microbiota can communicate modify host responses examined by describing recognition patterns, microbially derived epigenome effector proteins gene regulation. Finally, power omics tools used study highlighted emphasis integrated host-microbiota multiomics framework understand underlying during change-driven dysbiosis.

Language: Английский

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Triggers, cascades, and endpoints: connecting the dots of coral bleaching mechanisms

Biological reviews/Biological reviews of the Cambridge Philosophical Society, Journal Year: 2024, Volume and Issue: 99(3), P. 715 - 752

Published: Jan. 12, 2024

ABSTRACT The intracellular coral–dinoflagellate symbiosis is the engine that underpins success of coral reefs, one most diverse ecosystems on planet. However, breakdown and loss microalgal symbiont (i.e. bleaching) due to environmental changes are resulting in rapid degradation reefs globally. There an urgent need understand cellular physiology bleaching at mechanistic level help develop solutions mitigate reef crisis. Here, unprecedented scope, we present novel models integrate putative mechanisms within a common framework according triggers (initiators bleaching, e.g. heat, cold, light stress, hypoxia, hyposalinity), cascades (cellular pathways, photoinhibition, unfolded protein response, nitric oxide), endpoints (mechanisms loss, apoptosis, necrosis, exocytosis/vomocytosis). supported by direct evidence from cnidarian systems, indirectly through comparative evolutionary analyses non‐cnidarian systems. With this approach, new have been established between initiated different triggers. In particular, provide insights into poorly understood connections highlight role mechanism i.e. ‘symbiolysosomal digestion’, which symbiophagy. This review also increases approachability for specialists non‐specialists mapping vast landscape atlas comprehensible detailed models. We then discuss major knowledge gaps how future research may improve understanding cascade pathways (endpoints).

Language: Английский

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Photosymbiosis shaped animal genome architecture and gene evolution as revealed in giant clams

Communications Biology, Journal Year: 2025, Volume and Issue: 8(1)

Published: Jan. 4, 2025

Abstract Symbioses are major drivers of organismal diversification and phenotypic innovation. However, how long-term symbioses shape whole genome evolution in metazoans is still underexplored. Here, we use a giant clam ( Tridacna maxima ) to demonstrate symbiosis has left complex signatures an animal’s genome. Giant clams thrive oligotrophic waters by forming remarkable association with photosymbiotic dinoflagellate algae. Genome-based demographic inferences uncover tight correlation between T. global population change paleoclimate habitat shifts, revealing abiotic biotic factors may dictate microevolution. Comparative analyses reveal genomic features that be symbiosis-driven, including expansion contraction immunity-related gene families large proportion lineage-specific genes. Strikingly, about 70% the composed repetitive elements, especially transposable most likely resulting from symbiosis-adapted immune system. This work greatly enhances our understanding underlie metazoan diversification.

Language: Английский

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The Molecular Language of the Cnidarian–Dinoflagellate Symbiosis

Trends in Microbiology, Journal Year: 2020, Volume and Issue: 29(4), P. 320 - 333

Published: Oct. 8, 2020

Language: Английский

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Comparison of 15 dinoflagellate genomes reveals extensive sequence and structural divergence in family Symbiodiniaceae and genus Symbiodinium

BMC Biology, Journal Year: 2021, Volume and Issue: 19(1)

Published: April 13, 2021

Abstract Background Dinoflagellates in the family Symbiodiniaceae are important photosynthetic symbionts cnidarians (such as corals) and other coral reef organisms. Breakdown of coral-dinoflagellate symbiosis due to environmental stress (i.e. bleaching) can lead death potential collapse ecosystems. However, evolution genomes, its implications for coral, is little understood. Genome sequences remain scarce part their large genome sizes (1–5 Gbp) idiosyncratic features. Results Here, we present de novo assemblies seven members genus Symbiodinium , which two free-living, one an opportunistic symbiont, remainder mutualistic symbionts. Integrating available data, compare 15 dinoflagellate genomes revealing high sequence structural divergence. Divergence among some isolates comparable that distinct genera Symbiodiniaceae. We also recovered hundreds gene families specific each lineage, many encode unknown functions. An in-depth comparison between symbiotic tridacnidorum (isolated from a coral) free-living natans reveals greater prevalence transposable elements, genetic duplication, rearrangements, pseudogenisation species. Conclusions Our results underscore impact lifestyle on lineage-specific gene-function innovation, divergence, diversification The divergent features report, putative causes, may apply microbial eukaryotes have undergone phases evolutionary history.

Language: Английский

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Insights into coral bleaching under heat stress from analysis of gene expression in a sea anemone model system

Proceedings of the National Academy of Sciences, Journal Year: 2020, Volume and Issue: 117(46), P. 28906 - 28917

Published: Nov. 9, 2020

Significance Coral reefs are biodiversity hotspots of great ecological, economic, and aesthetic importance. Their global decline under climate change other stresses makes it urgent to understand the molecular bases their responses stress, including “bleaching,” in which corals' photosynthetic algal symbionts lost, thus depriving host animals a crucial source energy metabolic building blocks. We sought clues mechanisms that cause (or protect against) bleaching by analyzing patterns gene expression sea anemone relative corals during exposure heat stress sufficient induce bleaching. The results challenge some current ideas about while also suggesting hypotheses identifying genes prime targets for future genetic analyses.

Language: Английский

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Thermotolerant coral symbionts modulate heat stress‐responsive genes in their hosts

Molecular Ecology, Journal Year: 2020, Volume and Issue: 29(15), P. 2940 - 2950

Published: June 25, 2020

Abstract Some corals may become more resistant to bleaching by shuffling their Symbiodiniaceae communities toward thermally tolerant species, and manipulations boost the abundance of these symbionts in increase resilience warming oceans. However, thermotolerant symbiont Durusdinium trenchii reduce growth fecundity Caribbean corals, tradeoffs need be better understood as this spreads through region. We sought understand how D. modulates coral gene expression manipulating Montastraea cavernosa produce replicate ramets containing together with paired same genets ( n = 3) Cladocopium C3 symbionts. then examined differences global between hosting under control temperatures, response short‐term heat stress. identified numerous transcriptional associated identity, which explained 2%–14% variance. Corals upregulated genes related translation, ribosomal structure biogenesis, downregulated extracellular structures, carbohydrate lipid transport metabolism, relative . Unexpectedly, changes were similar those observed Cladocopium‐ dominated stress, suggesting that cause stress‐responsive genes, explaining both increased tolerance energetic These findings provide insight into ecological occurring on contemporary reefs climate change, diverse ways different modulate emergent phenotypes hosts.

Language: Английский

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Dual RNA‐sequencing analyses of a coral and its native symbiont during the establishment of symbiosis

Molecular Ecology, Journal Year: 2020, Volume and Issue: 29(20), P. 3921 - 3937

Published: Aug. 28, 2020

Despite the ecological significance of mutualistic relationship between Symbiodiniaceae and reef-building corals, molecular interactions during establishment this are not well understood. This is particularly true transcriptional changes that occur in symbiont. In current study, a dual RNA-sequencing approach was used to better understand on both sides coral-symbiont interaction colonization Acropora tenuis by compatible strain (Cladocopium goreaui; ITS2 type C1). Comparison transcript levels hospite symbiont 3, 12, 48 72 hr after exposure those same culture revealed extensive generalized down-regulation gene expression occurred infection process. Included "symbiosis-derived repression" were range stress response immune-related genes. contrast, suite genes implicated metabolism upregulated symbiotic state. The coral data support hypothesis immune-suppression arrest phagosome maturation play important roles symbioses, additionally imply involvement some SCRiP family members Consistent with previous studies, transcriptomic suggest active translocation metabolites host may begin early process, thus can be established at larval stage. study provides insights into remodelling occurs C. goreaui transition lifestyle novel symbiosis.

Language: Английский

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Symbiosis maintenance in the facultative coral, Oculina arbuscula, relies on nitrogen cycling, cell cycle modulation, and immunity

Scientific Reports, Journal Year: 2021, Volume and Issue: 11(1)

Published: Oct. 27, 2021

Symbiosis with unicellular algae in the family Symbiodiniaceae is common across tropical marine invertebrates. Reef-building corals offer a clear example of cellular dysfunction leading to dysbiosis that disrupts entire ecosystems process termed coral bleaching. Due their obligate symbiotic relationship, understanding molecular underpinnings sustain this symbiosis reef-building challenging, as any aposymbiotic state inherently coupled severe physiological stress. Here, we leverage subtropical, facultatively and calcifying Oculina arbuscula investigate gene expression differences between branches within same colonies under baseline conditions. We further compare ontology (GO) KOG enrichment patterns from O. prior work sea anemone Exaiptasia pallida (Aiptasia) salamander Ambystoma maculatum-both which exhibit endophotosymbiosis algae. identify nitrogen cycling, cell cycle control, immune responses key pathways involved maintenance Understanding mechanisms healthy urgent importance given vulnerability these partnerships changing environmental conditions role continued functioning critical highly diverse ecosystems.

Language: Английский

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Harnessing the Power of Model Organisms To Unravel Microbial Functions in the Coral Holobiont

Microbiology and Molecular Biology Reviews, Journal Year: 2022, Volume and Issue: 86(4)

Published: Oct. 26, 2022

Stony corals build the framework of coral reefs, ecosystems immense ecological and economic importance. The existence these is threatened by climate change other anthropogenic stressors that manifest in microbial dysbiosis such as bleaching disease, often leading to mortality. Despite a significant amount research, mechanisms ultimately underlying destructive phenomena, what could prevent or mitigate them, remain be resolved. This mostly due practical challenges experimentation on highly complex nature holobiont also includes bacteria, archaea, protists, viruses. While overall importance partners well recognized, their specific contributions functioning interspecific dynamics largely unexplored. Here, we review potential adopting model organisms more tractable systems address knowledge gaps. We draw parallels from broader biological biomedical fields guide establishment, implementation, integration new emerging with aim addressing needs research. evaluate cnidarian models Hydra, Aiptasia, Cassiopea, Astrangia poculata; fast-evolving field tissue cell cultures; propose for establishment "true" tropical reef-building models. Based this assessment, suggest future research key aspects limiting our ability understand hence improve response ocean conditions.

Language: Английский

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