Cobalt Resistance via Detoxification and Mineralization in the Iron-Reducing Bacterium Geobacter sulfurreducens

Abstract

Bacteria in the genus Geobacter thrive in iron- and manganese-rich environments where the divalent cobalt cation (CoII) accumulates to potentially toxic concentrations. Consistent with selective pressure from environmental exposure, the model laboratory representative Geobacter sulfurreducens grew with CoCl2 concentrations (1 mM) typically used to enrich for metal-resistant bacteria from contaminated sites. We reconstructed from genomic data canonical pathways for CoII import and assimilation into cofactors (cobamides) that support the growth of numerous syntrophic partners. We also identified several metal efflux pumps, including one that was specifically upregulated by CoII. Cells acclimated to metal stress by downregulating non-essential proteins with metals and thiol groups that CoII preferentially targets. They also activated sensory and regulatory proteins involved in detoxification as well as pathways for protein and DNA repair. In addition, G. sulfurreducens upregulated respiratory chains that could have contributed to the reductive mineralization of the metal on the cell surface. Transcriptomic evidence also revealed pathways for cell envelope modification that increased metal resistance and promoted cell-cell aggregation and biofilm formation in stationary phase. These complex adaptive responses confer on Geobacter a competitive advantage for growth in metal-rich environments that are essential to the sustainability of cobamide-dependent microbiomes and the sequestration of the metal in hitherto unknown biomineralization reactions.

Geobacter sulfurreducens’ unique metabolism results in cells with a high iron and lipid content

“…Nickel is a cofactor in Ni-Fe hydrogenases, and the genome of G. sulfurreducens encodes for several (50, 51). G. sulfurreducens is able to assimilate cobalt through its cobamide-synthesis pathways (52), but it may also be precipitated on the cell surface as a defense mechanism against cobalt toxicity (53).…”

Selective bacterial separation of critical metals a sustainable method for recycling lithium ion batteries

“…1579 proteins were identified in this study which corresponds to of the total proteome of D. alaskensis G20, 22 providing comprehensive coverage of the bacterial response to the presence of these two transition metals, relative to previous studies. 21,23 Overall, higher similarities were found between the control and Co treatments compared to Ni-containing treatments, according to the specific protein abundance profiling especially after 2 h metal incubation (ANOVA, p-value < 0.05, peptide number ≥ 2, absolute ratio abundance >1.5). After 2 h incubation there was a remarkable reduction in the protein abundance in treatments containing 100 ppm of Ni 2+ in comparison to the control.…”

“…The synthesis of biogenic zero-valent Co NPs by the bacterium Geobacter sulfurreducens had been previously speculated but not demonstrated. 23 The biological mechanisms involved in the formation of zero-valent Co NPs are unknown and deserve further investigation, but have commenced with the proteomics work presented in this study. From these we hypothesise that certain proteins, including the quinoneinteracting membrane-bound oxidoreductase (Dde_1113), are involved in the reduction of Co 2+ to Co 0 and that other metal-binding affinity proteins in the membrane (Dde_0155, Dde_2208, Dde_3518) may play a role in the nucleation of Co resulting in nanoparticle formation.…”

Selective bacterial separation of critical metals: a sustainable method for recycling lithium ion batteries

“…1579 proteins were identified in this study which corresponds to 52% of the total proteome of D. alaskensis G20, 22 providing comprehensive coverage of the bacterial response to the presence of these two transition metals, relative to previous studies. 21,23 Overall, higher similarities were found between the control and Co treatments compared to Ni-containing treatments, according to the specific protein abundance profiling especially after 2 h metal incubation (ANOVA, p-value < 0.05, peptide number ≥ 2, absolute ratio abundance >1.5). After 2 h incubation there was a remarkable reduction in the protein abundance in treatments containing 100 ppm of Ni 2+ in comparison to the control.…”