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A Multi-Omics Analysis Suggests Links Between the Differentiated Surface Metabolome and Epiphytic Microbiota Along the Thallus of a Mediterranean Seaweed Holobiont.

ABSTRACT: Marine macroalgae constitute an important living resource in marine ecosystems and complex ecological interactions occur at their surfaces with microbial communities. In this context, the present study aimed to investigate how the surface metabolome of the algal holobiont Taonia atomaria could drive epiphytic microbiota variations at the thallus scale. First, a clear discrimination was observed between algal surface, planktonic and rocky prokaryotic communities. These data strengthened the hypothesis of an active role of the algal host in the selection of epiphytic communities. Moreover, significant higher epibacterial density and ?-diversity were found at the basal algal parts compared to the apical ones, suggesting a maturation gradient of the community along the thallus. In parallel, a multiplatform mass spectrometry-based metabolomics study, using molecular networking to annotate relevant metabolites, highlighted a clear chemical differentiation at the algal surface along the thallus with similar clustering as for microbial communities. In that respect, higher amounts of sesquiterpenes, phosphatidylcholines (PCs), and diacylglycerylhydroxymethyl-N,N,N-trimethyl-?-alanines (DGTAs) were observed at the apical regions while dimethylsulfoniopropionate (DMSP) and carotenoids were predominantly found at the basal parts of the thalli. A weighted UniFrac distance-based redundancy analysis linking the metabolomics and metabarcoding datasets indicated that these surface compounds, presumably of algal origin, may drive the zonal variability of the epibacterial communities. As only few studies were focused on microbiota and metabolome variation along a single algal thallus, these results improved our understanding about seaweed holobionts. Through this multi-omics approach at the thallus scale, we suggested a plausible scenario where the chemical production at the surface of T. atomaria, mainly induced by the algal physiology, could explain the specificity and the variations of the surface microbiota along the thallus.

SUBMITTER: Paix B

PROVIDER: S-EPMC7111306 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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A Multi-Omics Analysis Suggests Links Between the Differentiated Surface Metabolome and Epiphytic Microbiota Along the Thallus of a Mediterranean Seaweed Holobiont.

Paix Benoît B Carriot Nathan N Barry-Martinet Raphaëlle R Greff Stéphane S Misson Benjamin B Briand Jean-François JF Culioli Gérald G

Frontiers in microbiology 20200325

Marine macroalgae constitute an important living resource in marine ecosystems and complex ecological interactions occur at their surfaces with microbial communities. In this context, the present study aimed to investigate how the surface metabolome of the algal holobiont <i>Taonia atomaria</i> could drive epiphytic microbiota variations at the thallus scale. First, a clear discrimination was observed between algal surface, planktonic and rocky prokaryotic communities. These data strengthened th ...[more]

PMID: 32269559

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Project description:Terrestrial plants are known to "garden" the microbiota of their rhizosphere via released metabolites (that can attract beneficial microbes and deter pathogenic microbes). Such a "gardening" capacity is also known to be dynamic in plants. Although microbial "gardening" has been recently demonstrated for seaweeds, we do not know whether this capacity is a dynamic property in any aquatic flora like in terrestrial plants. Here, we tested the dynamic microbial "gardening" capacity of seaweeds using the model invasive red seaweed Agarophyton vermiculophyllum. Following an initial extraction of surface-associated metabolites (immediately after field collection), we conducted a long-term mesocosm experiment for 5 months to test the effect of two different salinities (low = 8.5 and medium = 16.5) on the microbial "gardening" capacity of the alga over time. We tested "gardening" capacity of A. vermiculophyllum originating from two different salinity levels (after 5 months treatments) in settlement assays against three disease causing pathogenic bacteria and seven protective bacteria. We also compared the capacity of the alga with field-collected samples. Abiotic factors like low salinity significantly increased the capacity of the alga to deter colonization by pathogenic bacteria while medium salinity significantly decreased the capacity of the alga over time when compared to field-collected samples. However, capacity to attract beneficial bacteria significantly decreased at both tested salinity levels when compared to field-collected samples. Dynamic microbial "gardening" capacity of a seaweed to attract beneficial bacteria and deter pathogenic bacteria is demonstrated for the first time. Such a dynamic capacity as found in the current study could also be applicable to other aquatic host-microbe interactions. Our results may provide an attractive direction of research towards manipulation of salinity and other abiotic factors leading to better defended A. vermiculophyllum towards pathogenic bacteria thereby enhancing sustained production of healthy A. vermiculophyllum in farms.

Project description:BackgroundAlthough considered as holobionts, macroalgae and their surface microbiota share intimate interactions that are still poorly understood. Little is known on the effect of environmental parameters on the close relationships between the host and its surface-associated microbiota, and even more in a context of coastal pollutions. Therefore, the main objective of this study was to decipher the impact of local environmental parameters, especially trace metal concentrations, on an algal holobiont dynamics using the Phaeophyta Taonia atomaria as a model. Through a multidisciplinary multi-omics approach combining metabarcoding and untargeted LC-MS-based metabolomics, the epibacterial communities and the surface metabolome of T. atomaria were monitored along a spatio-temporal gradient in the bay of Toulon (Northwestern Mediterranean coast) and its surrounding. Indeed, this geographical area displays a well-described trace metal gradient particularly relevant to investigate the effect of such pollutants on marine organisms.ResultsEpibacterial communities of T. atomaria exhibited a high specificity whatever the five environmentally contrasted collecting sites investigated on the NW Mediterranean coast. By integrating metabarcoding and metabolomics analyses, the holobiont dynamics varied as a whole. During the occurrence period of T. atomaria, epibacterial densities and α-diversity increased while the relative proportion of core communities decreased. Pioneer bacterial colonizers constituted a large part of the specific and core taxa, and their decrease might be linked to biofilm maturation through time. Then, the temporal increase of the Roseobacter was proposed to result from the higher temperature conditions, but also the increased production of dimethylsulfoniopropionate (DMSP) at the algal surface which could constitute of the source of carbon and sulfur for the catabolism pathways of these taxa. Finally, as a major result of this study, copper concentration constituted a key factor shaping the holobiont system. Thus, the higher expression of carotenoids suggested an oxidative stress which might result from an adaptation of the algal surface metabolome to high copper levels. In turn, this change in the surface metabolome composition could result in the selection of particular epibacterial taxa.ConclusionWe showed that associated epibacterial communities were highly specific to the algal host and that the holobiont dynamics varied as a whole. While temperature increase was confirmed to be one of the main parameters associated to Taonia dynamics, the originality of this study was highlighting copper-stress as a major driver of seaweed-epibacterial interactions. In a context of global change, this study brought new insights on the dynamics of a Mediterranean algal holobiont submitted to heavy anthropic pressures. Video abstract.

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Project description:Abstract In degraded coral reef ecosystems, allelopathic macroalgae have received increasing attention from marine ecologists because their secondary metabolites (also known as allelochemicals) kill corals that grow adjacent to them and weaken the recovery of degraded reefs. One well‐known coral‐killing macroalga is the calcareous red seaweed Galaxaura. However, our knowledge of how coral reef fishes interact with allelopathic algae like Galaxaura is very limited. Here, we documented novel observations of feeding interactions of 17 species of coral reef fishes (herbivorous and carnivorous) with the filamentous Galaxaura divaricata on degraded lagoon patch reefs in Dongsha Atoll (South China Sea). Video analyses showed that territorial farming damselfishes (i.e., Dischistodus perspicillatus, D. prosopotaenia, Hemiglyphidodon plagiometopon, Pomacentrus grammorhynchus, P. adelus, and Neoglyphidodon nigroris) and juvenile parrotfishes (Scarus schlegeli, S. ghobban, S. rivulatus, and Chlorurus spilurus) likely used G. divaricata as a feeding substratum. Further, microscopic analyses revealed that the filamentous surface of G. divaricata harbored a wealth of epiphytic microalgae, such as filamentous cyanobacteria (i.e., Leptolyngbya, Lyngbya, Rivularia, Oscillatoria, and Stigonema), diatoms (i.e., Synedra, Nitzschia, Mastogloia, and Pleurosigma), and filamentous red algae (i.e., Heterosiphonia), suggesting that these fishes targeted the nutrient‐rich microscopic epiphytes rather than the nutrient‐poor host. Juvenile benthic carnivores (i.e., Labridae, Parupeneus multifasciatus, and Meiacanthus grammistes) form feeding assemblages with roving parrotfishes to feed on small invertebrates (i.e., amphipods, copepods, isopods, gastropods, and polychaetes) associated with G. divaricata. Given that coral reef fishes appear to target the epiphytes associated with Galaxaura rather than the alga itself, these observations thus substantiate the threat posed by the overgrowth of G. divaricata to coral recovery in degraded reef systems due to the lack of natural grazers. Chemical‐rich allelopathic macroalgae are competing with corals in sub‐/tropical reef ecosystems. According to the prevailing view, these algae deter herbivores with their secondary metabolites. Contrary to this view we observed that allelopathic macroalgae like Galaxaura divaricata can provide a substratum for nutrient‐rich epiphytes that in turn present a food source for coral reef fishes. These observations suggest that Galaxaura may play an ecological role that has been overlooked and deserves our attention in the context of the resilience of coral reef ecosystems.

Dataset Information

A Multi-Omics Analysis Suggests Links Between the Differentiated Surface Metabolome and Epiphytic Microbiota Along the Thallus of a Mediterranean Seaweed Holobiont.

Publications

A Multi-Omics Analysis Suggests Links Between the Differentiated Surface Metabolome and Epiphytic Microbiota Along the Thallus of a Mediterranean Seaweed Holobiont.

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