Background Although 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. Results Epibacterial 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. Conclusion We 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.

the hulls could limit the undesirable effects but together increase the costs both in time and money. Consequently, biofouling is costing billions of dollars each year to naval industry. [8,9] When talking about colonization on marine sensors, Delauney et al. showed that biofouling affected the sensitivity and caused drift of measurements of the device over time. [10] Biofouling is also a big issue in the case of renewable marine energy devices. Biofouling on wave energy converters (WEC) leads to the decrease in efficiency of the devices by increasing drag and is also responsible of local biocorrosion. [11,12] The maintenance of such structure is risky and expensive, requiring period of good weather and calm sea state, among others. [13] Maintenance is all the more necessary during summer when fouling is the most intensive, due to higher seawater temperature, solar irradiation, and number of organisms. [13,14] In aquaculture, biofouling is also a major concern. Fitridge et al. reviewed all the effect of marine biofouling and its control in aquaculture. [15] Indeed, it can be responsible of cage deformation and structural fatigue, it will reduce the quality of water by limiting oxygen availability or increase the disease risk for fish species. Considering shellfish, biofouling can be responsible of mortality, shell erosion, competition for food and space, or disturbance in shell growth, for instance.In desalination plants, settlement, and accumulation of foulers onto the surface of the membranes or its pores lead to a deterioration of the filter. Salt rejection is negatively affected by the degradation of the membrane due to fouling. [16] Preventing fouling appears consequently a major concern for naval and marine industry, including sustainable domains like aquaculture, desalination plant, or the development of marine renewable energy devices.Protecting marine infrastructures has been the main matter of concern since the beginning of maritime transports. Tar, wax, arsenic, asphalt, or pitch are thought to be components used during antiquity for the first antifouling coatings. [3,5] Phoenicians and Carthaginians possibly used copper plates to protect their ships. [3,5] In the early 18th century, boats started to be made of steel. Zinc, nickel, and lead were chosen instead of copper plates to protect ships, because of corrosion matter. [3,17] From the late 18th century, heavy metal were more and more Marine biofouling is the unwanted accumulation of biological origin matters on submerged surfaces. Biofouling is a major economic burden on navy and commercial ships, as well as civil structures, piping systems, sensors, and power generating facilities. Due to the vast variety of marine organisms that colonize submerged surfaces, no surface has been found that is completely resistant to marine biofouling. The development of bioinspired and textured surfaces and their effects on marine biofouling are reviewed here. Different parameters such as mechanical properties, wettability, and surface topo graphy are shown to have...

Summary In the context of global warming, this study aimed to assess the effect of temperature and irradiance on the macroalgal Taonia atomaria holobiont dynamics. We developed an experimental set‐up using aquaria supplied by natural seawater with three temperatures combined with three irradiances. The holobiont response was monitored over 14 days using a multi‐omics approach coupling algal surface metabolomics and metabarcoding. Both temperature and irradiance appeared to shape the microbiota and the surface metabolome, but with a distinct temporality. Epibacterial community first changed according to temperature, and later in relation to irradiance, while the opposite occurred for the surface metabolome. An increased temperature revealed a decreasing richness of the epiphytic community together with an increase of several bacterial taxa. Irradiance changes appeared to quickly impact surface metabolites production linked with the algal host photosynthesis (e.g. mannitol, fucoxanthin, dimethylsulfoniopropionate), which was hypothesized to explain modifications of the structure of the epiphytic community. Algal host may also directly adapt its surface metabolome to changing temperature with time (e.g. lipids content) and also in response to changing microbiota (e.g. chemical defences). Finally, this study brought new insights highlighting complex direct and indirect responses of seaweeds and their associated microbiota under changing environments.

Marine biofouling communities, including biofilms, are composed of many eukaryotes with high taxonomic and functional diversities. However, molecular characterization of eukaryotic diversity of marine biofouling has been barely developed due to the only recent interest in research areas such as marine renewable energies, antifouling technologies, or plastic pollution. The aim of this study was to compare the diversity and taxonomic composition of biofouling through different metabarcoding approaches used to detect the widest range of taxa from samples collected in several contrasted marine environments (French Atlantic and Mediterranean coasts). Thus, we assessed four DNA extraction methods and six primers pairs targeting the 18S rDNA gene (including the V1-V2, V4TAR, V4UNI, V7 and V9 regions) and the COI gene, the latter with two databases (BOLD and MIDORI). In addition the influence of primers selection was analyzed at three sites to compare geographic variations in eukaryotic diversity. Although none of the extraction methods greatly altered the community diversity or composition. we have observed that eukaryotic biofouling community diversity and structure varied depending on primers pairs, reference databases and sites. 18S rDNA regions allowed the detection of more taxa at the species level, including microeukaryotes, while the COI recovered more ASVs, but with a large proportion that remained taxonomically unassigned probably because BOLD and MIDORI specifically targeted metazoans. Interestingly, the spatial pattern obtained with both COI and 18S rDNA markers were similar showing that spatial selection occurred throughout a wide diversity of eukaryotic taxa. These results encouraged the use of these two complementary markers for future metabarcoding investigations but also highlighted the relevance of completing databases to enhance the identification of biofouling eukaryotes.

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