Isolation of an antimicrobial compound produced by bacteria associated with reef-building corals

Raina, Jean‐Baptiste; Tapiolas, Dianne M.; Motti, Cherie A.; Fôret, Sylvain; Seemann, Torsten; Tebben, Jan; Willis, Bette L.; Bourne, David G.

doi:10.7287/peerj.preprints.2282v1

Cited by 22 publications

(41 citation statements)

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“…In terms of S cycling, there was overlap in coverage of S related pathways in the two host species, although some pathways were more complete in X. muta than M. cavernosa. No transcripts corresponding to dimethylsulfoniopropionate (DMSP) production were observed in M. cavernosa, which was expected as this pathway is thought to be driven by Symbiodiniaceae 41 and those eukaryotic transcripts were not included in this analysis. While both hosts expressed sulfate assimilation genes, only M. cavernosa expressed sulfate transport and only X. muta expressed sulfur oxidation genes and other sulfur metabolism genes such as alkanesulfonate monoxygenase (ssuD, Fig.…”

Section: Functional Overview Of the Sponge And Coral Microbiome Profmentioning

confidence: 99%

Trait-Based Comparison of Coral and Sponge Microbiomes

Fiore

Jarett

Steinert

et al. 2020

Sci Rep

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corals and sponges harbor diverse microbial communities that are integral to the functioning of the host. While the taxonomic diversity of their microbiomes has been well-established for corals and sponges, their functional roles are less well-understood. It is unclear if the similarities of symbiosis in an invertebrate host would result in functionally similar microbiomes, or if differences in host phylogeny and environmentally driven microhabitats within each host would shape functionally distinct communities. Here we addressed this question, using metatranscriptomic and 16S rRNA gene profiling techniques to compare the microbiomes of two host organisms from different phyla. Our results indicate functional similarity in carbon, nitrogen, and sulfur assimilation, and aerobic nitrogen cycling. Additionally, there were few statistical differences in pathway coverage or abundance between the two hosts. For example, we observed higher coverage of phosphonate and siderophore metabolic pathways in the star coral, Montastraea cavernosa, while there was higher coverage of chloroalkane metabolism in the giant barrel sponge, Xestospongia muta. Higher abundance of genes associated with carbon fixation pathways was also observed in M. cavernosa, while in X. muta there was higher abundance of fatty acid metabolic pathways. Metagenomic predictions based on 16S rRNA gene profiling analysis were similar, and there was high correlation between the metatranscriptome and metagenome predictions for both hosts. our results highlight several metabolic pathways that exhibit functional similarity in these coral and sponge microbiomes despite the taxonomic differences between the two microbiomes, as well as potential specialization of some microbially based metabolism within each host. Microbial symbionts have played a critical role in shaping the evolution of multicellular life by facilitating and promoting host defense 1 , nutrient acquisition 2 , and species diversification 3. For example, in coral reef ecosystems, intracellular dinoflagellates in the Family Symbiodiniaceae occur as the primary mutualistic symbionts within the coral host and are essential to the survival and growth of the coral host, while receiving a suitable habitat and essential nutrients in return 4,5. Prokaryotic symbionts also contribute to the success of coral reef organisms, including corals and sponges 6-9 , by providing bioactive compounds for chemical defenses 10,11 , recycling host waste 12,13 , and in some cases providing a reliable source of vitamins and nutrients 14-17. Numerous studies have characterized the taxonomic composition of microbes in corals and sponges 18,19 ; however, our understanding of the multiple functional roles of these symbionts is still incomplete. Corals and sponges harbor remarkably diverse prokaryotic symbionts with thousands of unique taxa in many coral and sponge species 20,21. Many of these taxa persist across different host species (i.e., the core microbiome) over broad spatial scales 9,22-24 , and in some cases these host-...

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Section: Functional Overview Of the Sponge And Coral Microbiome Profmentioning

confidence: 99%

Trait-Based Comparison of Coral and Sponge Microbiomes

Fiore

Jarett

Steinert

et al. 2020

Sci Rep

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“…Only a few studies have specifically considered Symbiodiniaceae‐bacterial interactions in the coral holobiont, with their results pointing to the potentially critical role that these partnerships might play in regulating holobiont nutrient cycling and competitive fitness (Ritchie, ; Bourne et al ., ; Ainsworth et al ., ; Peixoto et al ., ; Silveira et al ., ; Bernasconi et al ., ); Table ). For example, some coral‐associated bacteria can rapidly take up organosulfur compounds released by Symbiodiniaceae cells, such as dimethylsulfoniopropionate (DMSP), to sustain their growth and produce an antimicrobial compound active against common coral pathogens (Raina et al ., ; Raina et al ., ). The stability of coral‐associated bacterial communities during thermal stress is correlated to the Symbiodiniaceae spp.…”

Section: Introductionmentioning

confidence: 99%

“…This resource exchange is one of the defining features allowing reef‐building corals to flourish in otherwise nutrient‐poor environments. Bacteria are also key ecological partners of cnidarians and are increasingly recognized as crucially important for the health of the holobiont (Bourne et al ., ; Raina et al ., ; Hernandez‐Agreda et al ., ; Peixoto et al ., ; Brener‐Raffalli et al ., ) (Fig. ).…”

Section: Introductionmentioning

confidence: 99%

Symbiodiniaceae‐bacteria interactions: rethinking metabolite exchange in reef‐building corals as multi‐partner metabolic networks

Matthews

Raina

Kahlke

et al. 2020

Environmental Microbiology

105

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Summary The intimate relationship between scleractinian corals and their associated microorganisms is fundamental to healthy coral reef ecosystems. Coral‐associated microbes (Symbiodiniaceae and other protists, bacteria, archaea, fungi and viruses) support coral health and resilience through metabolite transfer, inter‐partner signalling, and genetic exchange. However, much of our understanding of the coral holobiont relationship has come from studies that have investigated either coral‐Symbiodiniaceae or coral‐bacteria interactions in isolation, while relatively little research has focused on other ecological and metabolic interactions potentially occurring within the coral multi‐partner symbiotic network. Recent evidences of intimate coupling between phytoplankton and bacteria have demonstrated that obligate resource exchange between partners fundamentally drives their ecological success. Here, we posit that similar associations with bacterial consortia regulate Symbiodiniaceae productivity and are in turn central to the health of corals. Indeed, we propose that this bacteria‐Symbiodiniaceae‐coral relationship underpins the coral holobiont's nutrition, stress tolerance and potentially influences the future survival of coral reef ecosystems under changing environmental conditions. Resolving Symbiodiniaceae‐bacteria associations is therefore a logical next step towards understanding the complex multi‐partner interactions occurring in the coral holobiont.

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“…P12 isolated from P. damicornis is able to metabolize dimethylsulfoniopropionate to produce large amounts of tropodithietic acid, which shows strong antibacterial activity (MIC value 0·5 μg ml −1 ) against the coral pathogens V. coralliilyticus and V. owensii (Raina et al . 2016).…”

Section: Secondary Metabolites From Cabmentioning

confidence: 99%

Ecological and biotechnological importance of secondary metabolites produced by coral‐associated bacteria

et al. 2020

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Summary Symbiotic relationships between corals and their associated micro‐organisms are essential to maintain host homeostasis. Coral‐associated bacteria (CAB) can have different beneficial roles in the coral metaorganism, such as metabolizing essential nutrients for the coral host and protecting the coral from pathogens. Many CAB exert these functions via secondary metabolites, which include antibacterial, antifouling, antitumour, antiparasitic and antiviral compounds. This review describes how analysis of CAB has led to the discovery of secondary metabolites with potential biotechnological applications. The most commonly found types of secondary metabolites, antimicrobial and antibiofilm compounds, are emphasized and described. Recently developed methods that can be applied to enhance the culturing of CAB from shallow‐water reefs and the less‐studied deep‐sea coral reefs are also discussed. Last, we suggest how the combined use of meta‐omics and innovative growth‐diffusion techniques can vastly improve the discovery of novel compounds in coral environments.

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Isolation of an antimicrobial compound produced by bacteria associated with reef-building corals

Cited by 22 publications

References 0 publications

Trait-Based Comparison of Coral and Sponge Microbiomes

Trait-Based Comparison of Coral and Sponge Microbiomes

Symbiodiniaceae‐bacteria interactions: rethinking metabolite exchange in reef‐building corals as multi‐partner metabolic networks

Ecological and biotechnological importance of secondary metabolites produced by coral‐associated bacteria

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