Time-resolved analysis of a denitrifying bacterial community revealed a core microbiome responsible for the anaerobic degradation of quinoline

Abstract

Quinoline is biodegradable under anaerobic conditions, but information about the degradation kinetics and the involved microorganisms is scarce. Here, the dynamics of a quinoline-degrading bacterial consortium were studied in anoxic batch cultures containing nitrate. The cultures removed 83.5% of the quinoline during the first 80 hours, which were dominated by denitrification, and then switched to methanogenesis when the nitrogen oxyanions were depleted. Time-resolved community analysis using pyrosequencing revealed that denitrifiying bacteria belonging to the genus Thauera were enriched during the denitrification stage from 12.2% to 38.8% and 50.1% relative abundance in DNA and cDNA libraries, respectively. This suggests that they are key organisms responsible for the initial attack on quinoline. Altogether, 13 different co-abundance groups (CAGs) containing 76 different phylotypes were involved, directly or indirectly, in quinoline degradation. The dynamics of these CAGs show that specific phylotypes were associated with different phases of the degradation. Members of Rhodococcus and Desulfobacterium, as well as Rhodocyclaceae- and Syntrophobacteraceae-related phylotypes, utilized initial metabolites of the quinoline, while the resulting smaller molecules were used by secondary fermenters belonging to Anaerolineae. The concerted action by the different members of this consortium resulted in an almost complete anaerobic mineralization of the quinoline.

Cross-feeding betweenThauera aminoaromaticaandRhodococcus pyridinivoransdrove quinoline biodegradation in a denitrifying bioreactor

“…On the petri dish for bacteria isolation, a type of reddish colony frequently appeared. The identification by 16S rRNA gene suggested it represented another predominant bacterial phylotype for quinoline degradation proposed in previous literature (16). The isolate YF3 was selected as the representative of the most predominant Rhodococcus OTU, which was identified as Rhodococcus pyridinivorans .…”

“…To further identify the bacteria being responsible for transforming quinoline to 2-hydroxyquinoline, we further explored other key players from the predominant bacteria in the community. The members of genus Rhodococcus were known as aerobic quinoline degraders (8), and this phylotype has been reported closely related with quinoline denitrifying degradation (15, 16). Based on that, Rhodococcus pyridinivorans YF3 isolated from the bioreactor was considered as a candidate to initial attack for quinoline in the denitrifying bioreactor.…”

“…An efficient anoxic microbial community was enriched in a chemostat that was operated for more than 10 years with quinoline as electron donor and nitrate as electron acceptor. Phylogenetic analysis of this consortium showed that specific phylotypes were associated with different stages of the degradation (16), which suggests that microorganisms interact during quinoline metabolism. However, our understanding of this interaction is restricted due to the complexity of the community composition in the bioreactor while lack of anaerobic degrading microorganisms available in pure culture.…”

“…In addition, no evidence proved the role of main anaerobic degraders in these industrial bioreactors. There were several efforts to elucidate the anaerobic degraders by using the lab scale bioreactor and batch culture experiments (13–16). But to date, only one isolate, Desulfobacterium indolicum strain DSM 3383, which used sulfate as electron acceptor, was purely cultured as an anaerobic quinoline degrader (17).…”

“…To investigate the underlying microbial processes in this complex quinoline-degrading consortium, we endeavored to isolate the most predominant and active bacteria, which had been identified as the keystone organisms involved in denitrifying quinoline removal (16,18). The degradation characteristics of these isolates were evaluated under different conditions.…”