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Trace metal (TM) contamination in marine coastal areas is a worldwide threat for aquatic communities. However, little is known about the influence of a multi-chemical contamination on both marine biofilm communities’ structure and functioning. To determine how TM contamination potentially impacted microbial biofilms’ structure and their functions, polycarbonate (PC) plates were immerged in both surface and bottom of the seawater column, at five sites, along strong TM contamination gradients, in Toulon Bay. The PC plates were incubated during 4 weeks to enable colonization by biofilm-forming microorganisms on artificial surfaces. Biofilms from the PC plates, as well as surrounding seawaters, were collected and analyzed by 16S rRNA amplicon gene sequencing to describe prokaryotic community diversity, structure and functions, and to determine the relationships between bacterioplankton and biofilm communities. Our results showed that prokaryotic biofilm structure was not significantly affected by the measured environmental variables, while the functional profiles of biofilms were significantly impacted by Cu, Mn, Zn, and salinity. Biofilms from the contaminated sites were dominated by tolerant taxa to contaminants and specialized hydrocarbon-degrading microorganisms. Functions related to major xenobiotics biodegradation and metabolism, such as methane metabolism, degradation of aromatic compounds, and benzoate degradation, as well as functions involved in quorum sensing signaling, extracellular polymeric substances (EPS) matrix, and biofilm formation were significantly over-represented in the contaminated site relative to the uncontaminated one. Taken together, our results suggest that biofilms may be able to survive to strong multi-chemical contamination because of the presence of tolerant taxa in biofilms, as well as the functional responses of biofilm communities. Moreover, biofilm communities exhibited significant variations of structure and functional profiles along the seawater column, potentially explained by the contribution of taxa from surrounding sediments. Finally, we found that both structure and functions were significantly distinct between the biofilm and bacterioplankton, highlighting major differences between the both lifestyles, and the divergence of their responses facing to a multi-chemical contamination.

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 α-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-β-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.

While marine biofilms depend on environmental conditions and substrate, little is known about the influence of hydrodynamic forces. We tested different immersion modes (dynamic, cyclic and static) in Toulon Bay (north-western Mediterranean Sea; NWMS). The static mode was also compared between Toulon and Banyuls Bays. In addition, different artificial surfaces designed to hamper cell attachment (self-polishing coating: SPC; and fouling-release coating: FRC) were compared to inert plastic. Prokaryotic community composition was affected by immersion mode, surface characteristics and site. Rhodobacteriaceae and Flavobacteriaceae dominated the biofilm community structure, with distinct genera according to surface type or immersion mode. Cell density increased with time, greatly limited by hydrodynamic forces, and supposed to delay biofilm maturation. After 1 year, a significant impact of shear stress on the taxonomic structure of the prokaryotic community developed on each surface type was observed. When surfaces contained no biocides, roughness and wettability shaped prokaryotic community structure, which was not enhanced by shear stress. Conversely, the biocidal effect of SPC surfaces, already major in static immersion mode, was amplified by the 15 knots speed. The biofilm community on SPC was 60% dissimilar to the biofilm on the other surfaces and was distinctly colonized by Sphingomonadaceae ((Alter)Erythrobacter). At Banyuls, prokaryotic community structures were more similar between the four surfaces tested than at Toulon, due possibly to a masking effect of environmental constraints, especially hydrodynamic, which was greater than in Toulon. Finally, predicted functions such as cell adhesion confirmed some of the hypotheses drawn regarding biofilm formation over the artificial surfaces tested here.

Unraveling the relative importance of both environmental conditions and ecological processes regulating bacterioplankton communities is a central goal in microbial ecology. Marine coastal environments are among the most urbanized areas and as a consequence experience environmental pressures. The highly anthropized Toulon Bay (France) was considered as a model system to investigate shifts in bacterioplankton communities along natural and anthropogenic physicochemical gradients during a 1-month survey. In depth geochemical characterization mainly revealed strong and progressive Cd, Zn, Cu, and Pb contamination gradients between the entrance of the Bay and the north-western anthropized area. On the other hand, low-amplitude natural gradients were observed for other environmental variables. Using 16S rRNA gene sequencing, we observed strong spatial patterns in bacterioplankton taxonomic and predicted function structure along the chemical contamination gradient. Variation partitioning analysis demonstrated that multiple metallic contamination explained the largest part of the spatial biological variations observed, but DOC and salinity were also significant contributors. Network analysis revealed that biotic interactions were far more numerous than direct interactions between microbial groups and environmental variables. This suggests indirect effects of the environment, and especially trace metals, on the community through a few taxonomic groups. These spatial patterns were also partially found for predicted bacterioplankton functions, thus indicating a limited functional redundancy. All these results highlight both potential direct influences of trace metals contamination on coastal bacterioplankton and indirect forcing through biotic interactions and cascading.