Analysis of the impact of organic pollutants on marine microbial communities

Increasing amounts of organic synthetic chemicals are currently emitted to the environment by human activities. The more recalcitrant fraction of this pollutant mixture reaches marine ecosystems mainly through rivers, continental run-off, and diffuse atmospheric inputs. Once in seawater, it represents the anthropogenic fraction of the dissolved organic carbon (ADOC) pool. However, the total amount of ADOC is unknown, while its effects to ecosystems and detailed composition is largely unknown. Over the past decades, the scientific research effort has focused on the effects of organic pollutants (OPs) in marine biota, especially in oil spills events or under toxicological testing in laboratories, neglecting the importance of the chronic pollution perturbation of the biosphere composition caused by diffusive inputs of large number of pollutants at low concentrations. Our aim was to combine functional genomic tools with quantitative biogeochemical approaches under manipulated conditions to determine the bidirectional interaction between marine microbial community structure and function and the ADOC present in coastal seawater. Additionally, it was also intended to perform similar experiments in areas with diverse environmental conditions to elucidate the role of the trophic conditions and levels of pollutants in the response. In order to fulfil the proposed objectives, several OP amendment experiments were performed with different OP additions and contrasted seawater from the North-Western Mediterranean, the Arctic and the Antarctic. On the one hand, the effect caused by 4 families of pollutants individually (alkanes, polycyclic aromatic hydrocarbons, organophosphate esters and perfluoroalkyl substances (PFAS)) was tested in 5 marine bacterial communities of the NW Mediterranean, and the specific effect of perfluorooctanesulfonate (PFOS) and perfluorooctanoate acids (corresponding to the family of PFAS) in communities from Deception Island (Antarctica). On the other hand, experiments were conducted to observe the effect of an operationally defined ADOC, which consisted of the non-polar extract of seawater, to bacterial communities from coastal waters with very different starting environmental conditions (Livingston Island (Antarctica), Svalbard (Arctic), Barcelona and Blanes (Mediterranean)). The results suggest that the baseline ADOC pollution ubiquitously present in the oceans, two orders of magnitude lower than DOC, is modifying bacterial communities and its functionality. ADOC induced the growth of rare taxa, most of them known as pollutants degraders, but also modified the activity of some metabolic pathways from certain taxonomical groups, such as those related to hydrocarbon breakdown and PFOS desulfurization. Consequently, this work provided evidences that ADOC might be changing the dynamics of ocean biogeochemical cycles. The relevance of this perturbation will need to be constrained with future research. At the same time, marine microorganisms are adapted to modulate the concentration and state of incoming pollutants, as an example, we have observed a PFOS decrease in incubations with bacteria from Antarctic waters. However, the bidirectional interaction between ADOC and marine bacteria is closely related with environmental variables and conditions (nutrients availability, water temperature, etc.), as well previous exposure to pollutants probably facilitating an adaptation of the communities. In terms of the pool of ADOC, the same ADOC perturbation did not result in the same response for marine communities in the Mediterranean, Arctic and Antarctica. The suite of microbial responses are thus taxa and compound specific and besides the growth of the rare biosphere, range from degradation of pollutants, changes in the enzymatic activities, modification of the composition of the cell membranes and surface properties, compound specific stress responses, among others.