Effects of Ocean Warming on the Underexplored Members of the Coral Microbiome

Maire, Justin; Buerger, Patrick; Chan, Wing Yan; Deore, Pranali; Dungan, Ashley M.; Nitschke, Matthew R.; Oppen, Madeleine J. H. van

doi:10.1093/icb/icac005

Cited by 15 publications

(12 citation statements)

References 127 publications

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“…Finally, while chlamydiae are abundantly found in cnidarian metabarcoding studies, cnidarian samples often contain symbiotic microeukaryotes, such as fungi and protists (e.g. Symbiodiniaceae, Ostreobium , corallicolids, and chromerids) [ 2 , 73 ]. Chlamydiae have been detected in laboratory cultures of both Symbiodiniaceae and Ostreobium [ 19–23 ].…”

Section: Discussionmentioning

confidence: 99%

Chlamydiae in corals: shared functional potential despite broad taxonomic diversity

Maire,

Collingro,

Horn

et al. 2024

ISME Communications

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Cnidarians, such as corals and sea anemones, associate with a wide range of bacteria that have essential functions, including nutrient cycling and the production of antimicrobial compounds. Within cnidarians, bacteria can colonize all microhabitats including the tissues. Among them are obligate intracellular bacteria of the phylum Chlamydiota (chlamydiae) whose impact on cnidarian hosts and holobionts, especially corals, remain unknown. Here, we conducted a meta-analysis of previously published 16S rRNA gene metabarcoding data from cnidarians (e.g., coral, jellyfish, anemones), eight metagenome-assembled genomes (MAGs) of coral-associated chlamydiae, and one MAG of jellyfish-associated chlamydiae to decipher their diversity and functional potential. While the metabarcoding dataset showed an enormous diversity of cnidarian-associated chlamydiae, six out of nine MAGs were affiliated with the Simkaniaceae family. The other three MAGs were assigned to the Parasimkaniaceae, Rhabdochlamydiaceae, and Anoxychlamydiaceae, respectively. All MAGs lacked the genes necessary for an independent existence, lacking any nucleotide or vitamin and most amino acid biosynthesis pathways. Hallmark chlamydial genes, such as a type III secretion system, nucleotide transporters, and genes for host interaction, were encoded in all MAGs. Together these observations suggest an obligate intracellular lifestyle of coral-associated chlamydiae. No unique genes were found in coral-associated chlamydiae, suggesting a lack of host specificity. Additional studies are needed to understand how chlamydiae interact with their coral host, and other microbes in coral holobionts. This first study of the diversity and functional potential of coral-associated chlamydiae improves our understanding of both the coral microbiome and the chlamydial lifestyle and host range.

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Section: Discussionmentioning

confidence: 99%

Chlamydiae in corals: shared functional potential despite broad taxonomic diversity

Maire,

Collingro,

Horn

et al. 2024

ISME Communications

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“…The coral microbiome is influenced by many factors, including host developmental stage (Sharp et al 2012;Damjanovic et al 2020), spatial scales (e.g., across an individual (Rohwer et al 2002) or geographic regions (Williams et al 2022)), and environmental change (van Oppen and Blackall 2019; Voolstra and Ziegler 2020) -especially thermal stress (reviewed in Maire et al 2022). However, interactions between microbes and other holobiont partners is particularly important for understanding coral resilience.…”

Section: The Role Of the Microbiome In Coral Holobiont Phenotype And ...mentioning

confidence: 99%

Help Me, Symbionts, You’re My Only Hope: Approaches to Accelerate Our Understanding of Coral Holobiont Interactions

Bove¹,

Ingersoll²,

Davies³

2022

Preprint

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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.

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“…Scleractinian corals are foundation members of coral reefs, as their skeleton forms the reefs' three-dimensional structure that provides habitats for many reef-dwelling organisms and because they are the main primary producers on the reef. Corals rely on a wide range of microorganisms for their survival, including protists, bacteria, archaea, fungi, and viruses (3)(4)(5). Photosynthetic dinoflagellates of the Symbiodiniaceae family are by far the most studied coral-associated microorganisms.…”

Section: Introductionmentioning

confidence: 99%

Colocalization and potential interactions of Endozoicomonas and chlamydiae in microbial aggregates of the coral Pocillopora acuta

et al. 2023

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Corals are associated with a variety of bacteria, which occur in the surface mucus layer, gastrovascular cavity, skeleton, and tissues. Some tissue-associated bacteria form clusters, termed cell-associated microbial aggregates (CAMAs), which are poorly studied. Here, we provide a comprehensive characterization of CAMAs in the coral Pocillopora acuta . Combining imaging techniques, laser capture microdissection, and amplicon and metagenome sequencing, we show that (i) CAMAs are located in the tentacle tips and may be intracellular; (ii) CAMAs contain Endozoicomonas (Gammaproteobacteria) and Simkania (Chlamydiota) bacteria; (iii) Endozoicomonas may provide vitamins to its host and use secretion systems and/or pili for colonization and aggregation; (iv) Endozoicomonas and Simkania occur in distinct, but adjacent, CAMAs; and (v) Simkania may receive acetate and heme from neighboring Endozoicomonas . Our study provides detailed insight into coral endosymbionts, thereby improving our understanding of coral physiology and health and providing important knowledge for coral reef conservation in the climate change era.

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Effects of Ocean Warming on the Underexplored Members of the Coral Microbiome

Cited by 15 publications

References 127 publications

Chlamydiae in corals: shared functional potential despite broad taxonomic diversity

Chlamydiae in corals: shared functional potential despite broad taxonomic diversity

Help Me, Symbionts, You’re My Only Hope: Approaches to Accelerate Our Understanding of Coral Holobiont Interactions

Colocalization and potential interactions of Endozoicomonas and chlamydiae in microbial aggregates of the coral Pocillopora acuta

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