Deciphering the mechanisms for preferential tolerance of Escherichia coli BL21 to Cd(II) over Cu(II) and Ni(II): A combined physiological, biochemical, and multiomics perspective

Abstract

Environmental pollution severely affects ecological functions/health, and nondegradable pollutants such as heavy metals (HMs) cause significant damage to living organisms. Escherichia coli is one of the most studied life forms, and its response to oxidative stress is driven by a complex ensemble of mechanisms driven by transcriptomic-level adjustments. However, the magnitude of the physiological, metabolic, and biochemical alterations and their relationships with transcriptomic changes remain unclear. Studying the growth of E. coli in Cd-, Cu-, and Ni-polluted media at pH 5.0, we observed that (i) downregulation of the alkyl hydroperoxide complex, glutathione reductase, and glutathione S-transferase by Cd inhibited H2O2 degradation, and the accumulated H2O2 was respectively 2.7, 1.7, and 2.4 times greater than that in the control, Cu, and Ni treatments; (ii) Zn-associated resistance protein (ZraP) was the major scavenger of Cd, with a 140.7-fold increase in its expression; (iii) the P-type Cu+ transporter (CopA), multicopper oxidase (CueO), and heteromultimeric transport system (CusCBAF) controlled the excretion and detoxification of Cu; (iv) the Cd2+/Zn2+/Pb2+-exporting P-type ATPase (ZntA) and transcriptional activator ZntR were the major transporters of Ni; (v) Cd upregulated biofilm formation and synthesis of secondary metabolites more than Cu and Ni, which resulted in increased adsorption and improved tolerance; and (vi) the activity of superoxide dismutase in Cu-spiked cells was 153.2 %, 141.7 %, and 172.7 % higher and corresponded to 85.7 %, 524.5 %, and 491.5 % lower O2●⁻ in the control, Cd-, and Ni-spiked cells, respectively. This study reveals E. coli's preferential tolerance mechanisms to Cd rather than Cu and Ni and demonstrates mechanisms for its survival in highly polluted environments.

Keywords

• Heavy metal pollution
• Multiomics
• Microbial tolerance
• Multicopper oxidase, ZraP