Trace Metal Contamination Impacts Predicted Functions More Than Structure of Marine Prokaryotic Biofilm Communities in an Anthropized Coastal Area

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.