Endogenous biohydrogen from a rhizobium-legume association drives microbial biodegradation of polychlorinated biphenyl in contaminated soil

Abstract

Endogenous hydrogen (H2) is produced through rhizobium-legume associations in terrestrial ecosystems worldwide through dinitrogen fixation. In turn, this gas may alter rhizosphere microbial community structure and modulate biogeochemical cycles. However, very little is understood about the role that this H2 leaking to the rhizosphere plays in shaping the persistent organic pollutants degrading microbes in contaminated soils. Here, we combined DNA-stable isotope probing (DNA-SIP) with metagenomics to explore how endogenous H2 from the symbiotic rhizobium-alfalfa association drives the microbial biodegradation of tetrachlorobiphenyl PCB 77 in a contaminated soil. The results showed that PCB77 biodegradation efficiency increased significantly in soils treated with endogenous H2. Based on metagenomes of 13C-enriched DNA fractions, endogenous H2 selected bacteria harboring PCB degradation genes. Functional gene annotation allowed the reconstruction of several complete pathways for PCB catabolism, with different taxa conducting successive metabolic steps of PCB metabolism. The enrichment through endogenous H2 of hydrogenotrophic Pseudomonas and Magnetospirillum encoding biphenyl oxidation genes drove PCB biodegradation. This study proves that endogenous H2 is a significant energy source for active PCB-degrading communities and suggests that elevated H2 can influence the microbial ecology and biogeochemistry of the legume rhizosphere.

Keywords

• Biohydrogen
• Soil
• Legume-rhizobium symbiosis
• Polychlorinated biphenyls
• Biodegradation
• Stable isotope probing