4.8 Article

Linking Increased Isotope Fractionation at Low Concentrations to Enzyme Activity Regulation: 4-Cl Phenol Degradation by Arthrobacter chlorophenolicus A6

Journal

ENVIRONMENTAL SCIENCE & TECHNOLOGY
Volume 56, Issue 5, Pages 3021-3032

Publisher

AMER CHEMICAL SOC
DOI: 10.1021/acs.est.1c04939

Keywords

limits of biodegradation; mass transfer; enzyme regulation; cell wall permeability; chemostat; proteomics; isotope effect

Funding

  1. ERC [616861]
  2. European Research Council (ERC) [616861] Funding Source: European Research Council (ERC)

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This study investigates the adaptation of bacteria to low concentrations of pollutants by studying the degradation of 4-chlorophenol (4-CP) by Arthrobacter chlorophenolicus A6. The researchers found that at lower concentrations, there was an increase in isotope fractionation of 4-CP, indicating a change in enzyme activity. Surprisingly, high concentrations were associated with increased cell wall permeability. These findings suggest that bacteria adapt to low concentrations through regulation of enzyme activity and provide insights into bacterial adaptation mechanisms at low concentrations.
Slow microbial degradation of organic trace chemicals (micropollutants) has been attributed to either downregulation of enzymatic turnover or rate-limiting substrate supply at low concentrations. In previous biodegradation studies, a drastic decrease in isotope fractionation of atrazine revealed a transition from rate-limiting enzyme turnover to membrane permeation as a bottleneck when concentrations fell below the Monod constant of microbial growth. With degradation of the pollutant 4-chlorophenol (4-CP) by Arthrobacter chlorophenolicus A6, this study targeted a bacterium which adapts its enzyme activity to concentrations. Unlike with atrazine degradation, isotope fractionation of 4-CP increased at lower concentrations, from epsilon(C) = -1.0 +/- 0.5 parts per thousand in chemostats (D = 0.090 h(-1), 88 mg L-1) and epsilon(C) = -2.1 +/- 0.5 parts per thousand in batch (c(0) = 220 mg L-1) to epsilon(C) = -4.1 +/- 0.2 parts per thousand in chemostats at 90 mu g L-1. Surprisingly, fatty acid composition indicated increased cell wall permeability at high concentrations, while proteomics revealed that catabolic enzymes (CphCI and CphCII) were differentially expressed at D = 0.090 h(-1). These observations support regulation on the enzyme activity level-through either a metabolic shift between catabolic pathways or decreased enzymatic turnover at low concentrations-and, hence, reveal an alternative end-member scenario for bacterial adaptation at low concentrations. Including more degrader strains into this multidisciplinary analytical approach offers the perspective to build a knowledge base on bottlenecks of bioremediation at low concentrations that considers bacterial adaptation.

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