Differential interaction modes of As(III)/As(V) with microbial cell membrane induces opposite effects on organic contaminant biodegradation in groundwater

Abstract

Arsenic, a widespread toxic metalloid in groundwater, derives both from natural geological environment and industrial discharge, is extensively detected to be coexisting with organic contaminants, such as 2,4,6-trichlorophenol (TCP), a prior concerned pollutant. During biological remediation of groundwater, arsenic potentially intervenes microbial behaviors. This study found an opposite interference of arsenic in its two different valences (III and V) on the degradation of TCP by the functional bacteria, Sphingomonas fennica K101. As(III) inhibited TCP degradation in a concentration-dependent manner (from 0.1-10 mg/L), with a maximum inhibition rate of 35.5%, whereas As(V) exhibited promoting effects by 13.8% and 33.2% at 1 mg/L and 10 mg/L, respectively. Employing field emission transmission electron microscopy, quantum chemical calculations, fourier-transform ion cyclotron resonance mass spectrometry and metabolomic analysis, we unveil distinct interactions between cell membranes and arsenic in two valence states. Exposure to As(III) led to significant accumulation of As(III) in the cytoplasm, followed by interaction with intracellular ferritin (ferritin heavy chain 1), releasing iron ions and generating ROS. Subsequently, it induced ferroptosis and disrupted bacterial basal metabolism, thereby inhibiting TCP biodegradation. Oppositely, As(V) bound to a critical component sphingosine and triggered sphingosine polymerization, increasing membrane permeability, which was evidenced by measuring lactate dehydrogenase release. This process facilitated TCP transmembrane permeation by reducing membrane or extracellular secretion resistance. As(V) concurrently upregulated energy metabolism and accelerated TCP degradation. Our study elucidates the influence of prevalent arsenic on biodegradation efficacy, particularly amidst changing redox conditions associated with varying arsenic valences.

Keywords

• As(III)/As(V)
• 2,4–6-trichlorophenol biodegradation
• Sphingosine
• Ferroptosis
• Extracellular polymeric substances
• Microbial metabolome