Spatial Patterns of bphA Gene Diversity Reveal Local Adaptation of Microbial Communities to PCB and PAH Contaminants

Biphenyl dioxygenases, encoded by the bphA gene, initiate the oxidation of polychlorinated biphenyls (PCBs) and specify the substrate range of PCB congeners metabolized by bacteria. Increased bphA gene diversity within microbial communities may allow a broader range of PCB congeners to be catabolized, thus resulting in greater PCB degradation. To assess the role of PCBs in modulating bphA gene diversity, 16S ribosomal RNA (rRNA) gene and bphA environmental DNA libraries were generated from bacterial communities in sediments with a steep gradient of PCB contamination. Multiple measures of sequence diversity revealed greater heterogeneity of bphA sequences in polluted compared to unpolluted locations. Codon-based signatures of selection in bphA sequences provided evidence of purifying selection. Unifrac analysis of 16S rRNA sequences revealed independent taxonomic lineages from polluted and unpolluted locations, consistent with the presence of locally adapted bacterial communities. Phylogenetic analysis of bphA sequences indicated that dioxygenases from sediments were closely related to previously characterized dioxygenases that metabolize PCBs and polynuclear aromatic hydrocarbons (PAHs), consistent with high levels of these contaminants within the studied sediments. Structural analyses indicated that the BphA protein of Rhodococcus jostii, capable of metabolizing both PCBs and PAHs, provided a more optimal modeling template for bphA sequences reported in this study than a BphA homologue with more restricted substrate specificity. Results from this study suggest that PCBs and PAHs may drive local adaptation of microbial communities by acting as strong selective agents for biphenyl dioxygenases capable of metabolizing a wide range of congeners.