Quorum sensing-enhanced electron transfer in anammox consortia: A mechanism for improved resistance to variable-valence heavy metals

Abstract

Quorum sensing (QS) is recognized for enhancing bacterial resistance against heavy metals by regulating the production of extracellular substances that hinder metal penetration into the intracellular environment. However, it remains unclear whether QS contributes to resistance by regulating electron transfer, thereby transforming metals from more toxic to less toxic forms. This study investigated the regulatory mechanism of acyl-homoserine lactone (AHL)-mediated quorum sensing (QS) on electron transfer under As(III) and Cr(VI) stress. Metagenomic binning results revealed that Candidatus Brocadia sinica serves as a major contributor to AHL production for regulating heavy metal resistance, while other symbiotic bacteria offer complementary resistance pathways. In these bacteria, the AHL synthesis gene htdS plays a pivotal role in QS regulation of electron transfer and heavy metal resistance. Experimental findings demonstrated that AHL increased the electron transport system activity by 19.8%, and upregulated electron transfer gene expression by 1.1- to 6.9-fold. The enhanced electron transfer facilitated a 28.7% increase in the transformation of As(III) to less toxic As(V) and monomethylarsonic acid, ultimately achieving efficient nitrogen removal under As(III) stress. This study expands our understanding of how QS strengthens bacterial resistance to heavy metals, offering novel strategies for enhancing nitrogen removal of anammox in heavy metal-contaminated environments.