Soil pollution and physico-chemical properties steer the bacterial community structure in the uneven highly polluted SIN Brescia-Caffaro site.

Contaminants are strong ecological drivers steering the microbiome structure in polluted soils. Bioremediation relies on the residing microbial communities and their activity but can be limited by spatial heterogeneity of microbial populations, contaminants and soil chemistry. Studies aimed at identifying the drivers of microbiome selection are therefore pivotal to develop in-situ bioremediation technologies. In this perspective, the National Priority Site SIN Brescia-Caffaro (Italy) offers a fascinating natural laboratory due to its extremely high, old, mixed and uneven soil contamination by metals and organic pollutants, in particular polychlorinated biphenyls (PCBs). Aim of our study was to evaluate the spatial correlations between environmental factors (pollutant fingerprints and soil physico-chemical properties) and the soil microbial community structure. More than 120 soil samples were collected in three areas in the SIN-Caffaro along a tridimensional geostatistically conceived grid, and were analyzed to estimate the soil hydrolytic activity, the physico-chemical features and the concentration of metals and 79 PCB congeners. A cultivation-independent approach led to unravel the phylogenetic structure of the residing bacterial communities. By means of statistical analyses, we showed that significantly different bacterial communities were selected in the investigated areas within the SIN Brescia-Caffaro. Spatial distribution of bacterial populations within each site was significantly correlated with physico-chemical soil parameters and pollutant concentrations. Soil physico-chemical properties were also significantly correlated to the hydrolytic activity of the soil microbiome, a relevant indicator of soil quality and pollutant availability in historically contaminated sites. The results demonstrated that the soil properties and the contaminant profile in the SIN Brescia-Caffaro shaped the structure of the residing bacterial communities, leading to hypothesize that it drove the selection of populations able to degrade the contaminants. The detection in the SIN Brescia-Caffaro soils of the bphA gene, codifying for the biphenyl dioxygenase involved in the aerobic PCB degradation process, confirmed that they host an intrinsic natural attenuation potential, possibly exploitable for future remediation interventions. This study also highlighted the prospect of exploiting spatial patterns of bacterial diversity as proxies for monitoring polluted sites.