Nationwide screening of landfill-derived organohalide-respiring bacteria elucidates a unique cross-feeding interaction for microbial reductive dehalogenation

Abstract

Landfill as a major reservoir of organohalide pollutants provides a unique niche for selective enrichment of organohalide-respiring bacteria (OHRB), playing a critical role in cycling of anthropogenic organohalides in natural environments. Nonetheless, information on the landfill-derived OHRB and associated microbial interactions for microbial reductive dehalogenation remains unknown. In this study, dehalogenation microcosms were established with nationwide landfill leachate samples collected from 45 cities in China, which dechlorinated a common anthropogenic organohalide - tetrachloroethene - to chloroethenes in varied extent. Both the 16S rRNA gene amplicon-sequencing and metagenomics analyses suggested critical roles of unknown Dehalococcoidia and phylogenetically-diverse facultative OHRB in microbial reductive dehalogenation in landfills. Further culture-based interaction examination showed a complicated metabolic network among OHRB, sulfate-reducing bacteria, fermenting bacteria and methanogenic archaea. Particularly, the acetate competition between obligate/facultative OHRB and methanogens were shown to have a threshold concentration of 0.06/0.20 mM, above which the methanogenic Methanosarcina became more competitive, in contrast to the dominance of acetotrophy of obligate/facultative OHRB under the threshold concentration. Accordingly, the Methanosarcina and OHRB preferred acetate transfer from fermenting Clostridium and sulfate-reducing Desulfovibrio, respectively, which was determined by the “Maximum Power Principle” to maximize ecological fitness through optimizing energy utilization efficiency. This study provided the first insight into landfill-derived OHRB and their metabolic interactions with associated functional microorganisms, which could support future bioremediation of organohalide-contaminated landfills.