Cross-feeding between Thauera aminoaromatica and Rhodococcus pyridinivorans drove quinoline biodegradation in a denitrifying bioreactor

Abstract

The complex bacterial community is predominated by several taxa, such as Thauera and Rhodococcus, in a quinoline-degrading denitrifying bioreactor. Yet it remains unclear about how the interactions between the different bacteria mediate the quinoline metabolism in denitrifying condition. In this study, we designed a sequence-specific amplification to guide the isolation of the most predominant bacteria and obtained four strains of Thauera aminoaromatica, the representative of one key member in the bioreactor. Test on these isolates demonstrated that all of them were unable to strive on quinoline but could efficiently degrade 2-hydroxyquinoline, the hypothesized primary intermediate of quinoline catabolism, under nitrate-reducing condition. However, another isolate, Rhodococcus pyridinivorans YF3, corresponding to the second abundant taxon in the same bioreactor, was found to degrade quinoline via 2-hydroxyquinoline. The end products and removal rate of quinoline by isolate YF3 were largely varied with the quantity of available oxygen. Specifically, quinoline could only be converted into 2-hydroxyquinoline without further transformation under the condition with insufficient oxygen, e.g. less than 0.5% initial oxygen in the vials. However, if were aerobically pre-cultured in the medium with quinoline the resting cells of YF3 could anaerobically convert quinoline into 2-hydroxyquinoline. A two-strain consortium constructed with isolates from Thauera (R2) and Rhodococcus (YF3) demonstrated an efficient denitrifying degradation of quinoline. Thus, we experimentally proved that the metabolism interaction based on the 2-hydroxyquinoline cross-feeding between two predominant bacteria constituted the mainstream of quinoline degradation. This work sheds light on the understanding of mechanism of quinoline removal in the denitrifying bioreactor. ImportanceWe experimentally verified the most predominant Thauera sp. was indeed active degrader for the intermediate metabolites and the second abundant taxon Rhodococcus exerted, however, key function for opening the food box for a complex quinoline-degrading community. An ecological guild composed of two isolates was assembled, revealing the different roles of keystone organisms in the microbial community. This study, to our best knowledge, is the first report on the cross feeding between the initial attacker with unprofitable catalysis of reluctant heterocyclic compounds and the second bacterium which then completely degrade the compound transformed by the first bacterium. These results could be a significant step forward towards elucidation of microbial mechanism for quinoline denitrifying degradation.