Exploring bacterial community structure and function associated with polychlorinated biphenyl biodegradation in two hydrogen-amended soils

Abstract

Hydrogen (H2) is a universal energy source supplying survival energy for numerous microbial functions. Diffusive fluxes of H2 released by rhizobacterial symbiont nodules in which H2 is an obligate by-product of dinitrogen fixation may act as an additional energy input shaping microbial community structure and function in soils. However, the effects of H2 at the soil-nodule interface on soil contaminant degradation processes are poorly understood. Here, we mimicked the hydrogen conditions present at the soil-nodule interface (10,000 ppmv) to test the impact of elevated H2 concentrations on soil microbial removal of 3, 3′, 4, 4′-tetrachlorobiphenyl (PCB77) and examined the associated bacterial communities and their functions by conducting a microcosm experiment using two different soil types at three PCB contamination levels (0.5, 1.0 and 5.0 mg kg−1). After incubation for 84 days the PCB77 removal rates in the elevated H2 treatments in the Paddy soil were significantly promoted (by 4.88 to 6.41%) compared with the control (0.5 ppmv H2) but no significant effect was observed in a Fluvo-aquic soil. This is consistent with changes in the abundance of functional genes for PCB-degraders as shown by quantitative real-time PCR (Q-PCR) and phylogenetic investigation of bacterial communities by reconstruction of unobserved states (PICRUSt). 16S amplicon sequencing was conducted to explore bacterial community structure and correlate the genera to potential PCB degradation. The abundance of a total of four potentially PCB-degrading bacterial genera (Bacillus, Streptomyces, Ramlibacter and Paenibacillus) increased with increasing H2 level. In addition, the abundance of hydrogenase in the elevated H2 treatments was higher than in the control across different contamination levels in both soil types. Thus, elevated H2 stimulated soil PCB degradation with direct effects (aerobic PCB-degrading bacteria directly utilized H2 as an energy source for growth and thus enhanced PCB degradation efficiency) and indirect effects (aerobic PCB-degrading bacteria acted synergistically with other hydrogenotrophs to enhance PCB degradation efficiency by exchange of substances and energy). These results help to further understand the role of elevated hydrogen amendment in the PCB biodegradation process and provide evidence that H2 supports metabolic and energetic flexibility in microorganisms supplying a range of ecosystem services.