Humin oxidation drives microbial dehalogenation in oligotrophic environments

Abstract

Energy acquisition presents a fundamental constraint for microbial survival in oligotrophic environments. Although heterotrophic organohalide-respiring bacteria (OHRB) are known to perform reductive dehalogenation in organohalide-contaminated oligotrophic ecosystems, their energy metabolism remains poorly understood. Here, we report that Pseudomonas sp. CP-1, an OHRB, can directly oxidize humin from diverse oligotrophic aquifers to drive organohalide respiration. Spectroscopy, electrochemistry and metabolic profiling demonstrated that electrons stored in phenolic hydroxyl and amino groups of humin were utilized by strain CP-1 for organohalide respiration. Mutational and chemical inhibition studies identified an extracellular electron uptake pathway involving a multiheme cytochrome EeuP, which transfers extracellular electrons into the organohalide-respiratory chain, thereby coupling humin oxidation with reductive dehalogenation. Phylogenetic analyses revealed the widespread distribution of EeuP homologs across environmental bacterial taxa, implying a broader ecological relevance. This discovery sheds light on the hidden world of subsurface microbiology, with implications for understanding microbial energy metabolism in the energy-scarce environments.