Metabolic reconfigurations aimed at the detoxification of a multi-metal stress in Pseudomonas fluorescens: Implications for the bioremediation of metal pollutants

• Pseudomonas fluorescens survives a multi-metal challenge by reconfiguring its metabolic networks.
• The enhanced biogenesis of oxalate is pivotal for this process.
• The disparate metals (Al, Ga, Ca, Fe and Zn) were all precipitated complexed to oxalate.
• Acylating glyoxylate dehydrogenase and isocitrate lyase were critical in generating the dicarboxylic acid.
• Fine-tuning of metabolic networks may be pivotal in devising unique bioremediation technologies.

Although the ability of microbial systems to adapt to the toxic challenge posed by numerous metal pollutants individually has been well documented, there is little detailed information on how bacteria survive in a multiple-metal environment. Here we describe the metabolic reconfiguration invoked by the soil microbe Pseudomonas fluorescens in a medium with millimolar amounts of aluminum (Al), iron (Fe), gallium (Ga), calcium (Ca), and zinc (Zn). While enzymes involved in the production of NADH were decreased, there was a marked increase in enzymatic activities dedicated to NADPH formation. A modified tricarboxylic acid (TCA) cycle coupled to an alternate glyoxylate shunt mediated the synthesis of adenosine triphosphate (ATP) with the concomitant generation of oxalate. This dicarboxylic acid was a key ingredient in the sequestration of the metals that were detoxified as a lipid complex. It appears that the microbe favors this strategy as opposed to a detoxification process aimed at each metal separately. These findings have interesting implications for bioremediation technologies.