ABSTRACT
Syntrophy achieved via microbial cooperation is vital for anaerobic hydrocarbon degradation and methanogenesis. However, limited understanding of the metabolic division of labor and electronic interactions in electro-stimulated microbiota has impeded the development of enhanced biotechnologies for degrading hydrocarbons to methane. Here, compared to the non-electro-stimulated methanogenic toluene-degrading microbiota, electro-stimulation at 800 mV promoted toluene degradation and methane production efficiencies by 11.49 %-14.76 % and 75.58 %-290.11 %, respectively. Hydrocarbon-degrading gene bamA amplification and metagenomic sequencing analyses revealed that f_Syntrophobacteraceae MAG116 may act as a toluene degrader in the non-electro-stimulated microbiota, which was proposed to establish electron syntrophy with the acetoclastic methanogen Methanosarcina spp. (or Methanothrix sp.) through e-pili or shared acetate. In the electro-stimulated microbiota, 37.22 ± 4.33 % of Desulfoprunum sp. (affiliated f_Desulfurivibrionaceae MAG10) and 58.82 ± 3.74 % of the hydrogenotrophic methanogen Methanobacterium sp. MAG74 were specifically recruited to the anode and cathode, respectively. The potential electrogen f_Desulfurivibrionaceae MAG10 engaged in interspecies electron transfer with both syntroph f_Syntrophobacteraceae MAG116 and the anode, which might be facilitated by c-type cytochromes (e.g., ImcH, OmcT, and PilZ). Moreover, upon capturing electrons from the external circuit, the hydrogen-producing electrotroph Aminidesulfovibrio sp. MAG60 could share electrons and hydrogen with the methanogen Methanobacterium sp. MAG74, which uniquely harbored hydrogenase genes ehaA-R and ehbA-P. This study elucidates the microbial interaction mechanisms underlying the enhanced metabolic efficiency of the electro-stimulated methanogenic toluene-degrading microbiota, and emphasizes the significance of metabolic and electron syntrophic interactions in maintaining the stability of microbial community functionality.
Subject(s)
Methane , Microbiota , Toluene , Methane/metabolism , Toluene/metabolism , Biodegradation, EnvironmentalABSTRACT
Tetrabromobisphenol A (TBBPA), a widely used brominated flame retardant in electronics manufacturing, has caused global contamination due to improper e-waste disposal. Its persistence, bioaccumulation, and potential carcinogenicity drive studies of its transformation and underlying (a)biotic interactions. This study achieved an anaerobic enrichment culture capable of reductively dehalogenating TBBPA to the more bioavailable bisphenol A. 16S rRNA gene amplicon sequencing and quantitative PCR confirmed that successive dehalogenation of four bromide ions from TBBPA was coupled with the growth of both Dehalobacter sp. and Dehalococcoides sp. with growth yields of 5.0 ± 0.4 × 108 and 8.6 ± 4.6 × 108 cells per µmol Br- released (N = 3), respectively. TBBPA dehalogenation was facilitated by solid humin and reduced humin, which possessed the highest organic radical signal intensity and reducing groups -NH2, and maintained the highest dehalogenation rate and dehalogenator copies. Genome-centric metatranscriptomic analyses revealed upregulated putative TBBPA-dehalogenating rdhA (reductive dehalogenase) genes with humin amendment, cprA-like Dhb_rdhA1 gene in Dehalobacter species, and Dhc_rdhA1/Dhc_rdhA2 genes in Dehalococcoides species. The upregulated genes of lactate fermentation, de novo corrinoid biosynthesis, and extracellular electron transport in the humin amended treatment also stimulated TBBPA dehalogenation. This study provided a comprehensive understanding of humin-facilitated organohalide respiration.