Coupling between Nitrogen Fixation and Tetrachlorobiphenyl Dechlorination in a Rhizobium-Legume Symbiosis

Legume-rhizobium symbioses have the potential to remediate soils contaminated with chlorinated organic compounds. Here, the model symbiosis between Medicago sativa and Sinorhizobium meliloti was used to explore the relationships between symbiotic nitrogen fixation and transformation of tetrachlorobiphenyl PCB 77 within this association. 45-day-old seedlings in vermiculite were pretreated with 5 mg L-1 PCB 77 for 5 days. In PCB-supplemented nodules, addition of the nitrogenase enhancer molybdate significantly stimulated dechlorination by 7.2-fold and reduced tissue accumulation of PCB 77 (roots by 96% and nodules by 93%). Conversely, dechlorination decreased in plants exposed to a nitrogenase inhibitor (nitrate) or harboring nitrogenase-deficient symbionts (nifA mutant) by 29% and 72%, respectively. A range of dechlorinated products (biphenyl, methylbiphenyls, hydroxylbiphenyls, and trichlorobiphenyl derivatives) were detected within nodules and roots under nitrogen-fixing conditions. Levels of nitrogenase-derived hydrogen and leghemoglobin expression correlated positively with nodular dechlorination rates, suggesting a more reducing environment promotes PCB dechlorination. Our findings demonstrate for the first time that symbiotic nitrogen fixation acts as a driving force for tetrachlorobiphenyl dechlorination. In turn, this opens new possibilities for using rhizobia to enhance phytoremediation of halogenated organic compounds.