Summary
An integrative multi‐omics approach allowed monthly variations for a year of the surface metabolome and the epibacterial community of the Mediterranean Phaeophyceae Taonia atomaria to be investigated. The LC–MS‐based metabolomics and 16S rDNA metabarcoding data sets were integrated in a multivariate meta‐omics analysis (multi‐block PLS‐DA from the MixOmic DIABLO analysis) showing a strong seasonal covariation (Mantel test: p < 0.01). A network based on positive and negative correlations between the two data sets revealed two clusters of variables, one relative to the ‘spring period’ and a second to the ‘summer period’. The ‘spring period’ cluster was mainly characterized by dipeptides positively correlated with a single bacterial taxon of the Alteromonadaceae family (BD1‐7 clade). Moreover, ‘summer’ dominant epibacterial taxa from the second cluster (including Erythrobacteraceae, Rhodospirillaceae, Oceanospirillaceae and Flammeovirgaceae) showed positive correlations with few metabolites known as macroalgal antifouling defences [e.g. dimethylsulphoniopropionate (DMSP) and proline] which exhibited a key role within the correlation network. Despite a core community that represents a significant part of the total epibacteria, changes in the microbiota structure associated with surface metabolome variations suggested that both environment and algal host shape the bacterial surface microbiota.
This study aimed to improve understanding of the strategies developed by the Mediterranean seaweed Taonia atomaria to chemically control bacterial epibiosis. An experimental protocol was optimized to specifically extract algal surface-associated metabolites by a technique involving dipping in organic solvents whilst the integrity of algal cell membranes was assessed by fluorescent microscopy. This methodology was validated using mass spectrometry-based profiles of algal extracts and analysis of their principal components, which led to the selection of methanol as the extraction solvent with a maximum exposure time of 15 s. Six compounds (A-F) were identified in the resulting surface extracts. Two of these surface-associated compounds (B and C) showed selective anti-adhesion properties against reference bacterial strains isolated from artificial surfaces while remaining inactive against epibiotic bacteria of T. atomaria. Such specificity was not observed for commercial antifouling biocides and other molecules identified in the surface or whole-cell extracts of T. atomaria.
Marine microalgae and cyanobacteria have largely been studied for their biotechnological potential and proved their ability to produce a wide array of bioactive molecules. We investigated the antifouling potential of unexplored benthic tropical microalgae using anti-adhesion and toxicity bioassays against two major micro-and ma crobiofoulers, namely bacteria and barnacles. Fifty strains belonging to six phyla [Cyanobacteria, Miozoa (Dinoflagellata), Bacillariophyta, Cryptophyta, Rhodophyta and Haptophyta] were isolated from southwestern Islands of the Indian Ocean. They were chosen in order to represent as much as possible the huge biodiversity of such a rich tropical ecosystem. The associated chemodiversity was highlighted by both NMR-and LC-MS-based metabolomics. The screening of 84 algal fractions revealed that the anti-adhesion activity was concentrated in methanolic ones (i.e. 93% of all active fractions). Our results confirmed that microalgae constitute a promising source of natural antimicrofoulants as 17 out of the 30 active fractions showed high or very high capacity to inhibit the adhesion of three biofilm-forming marine bacteria. Dinoflagellate-derived fractions were the most active, both in terms of number and intensity. However, dinoflagellates were also more toxic and may not be suitable as a source of environmentally friendly antifouling compounds, in contrast to diatoms, e.g. Navicula mollis. The latter and two dinoflagellates of the genus Amphidinium also had interesting antisettlement activities while being moderately toxic to barnacle larvae. Our approach, combining the bioprospecting of a large number of tropical microalgae for their anti-settlement potential and metabolomics analyses, constituted a first step towards the discovery of alternative ecofriendly antifoulants.
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