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.
Highlights
Metal micronutrients such as nickel (NiII), cobalt (CoII), manganese (MnII), and iron (FeII) are essential for life yet toxic above relatively low concentrations (Buccella et al, 2019)
We identified in G. sulfurreducens complete NikMNQO and CbiMNQO importers, the most widespread prokaryotic systems for NiII and CoII uptake (Rodionov et al, 2006)
CoII could selectively outcompete NiII and enter the cytoplasm via the NikMNQO system. These importers are annotated as ATP-binding Cassette (ABC) transporters, but they are part of the prokaryotic family of energy-coupling factor (ECF) systems that transport watersoluble vitamins and cofactors (Cracan and Banerjee, 2013)
Summary
Metal micronutrients such as nickel (NiII), cobalt (CoII), manganese (MnII), and iron (FeII) are essential for life yet toxic above relatively low concentrations (Buccella et al, 2019). Microorganisms have evolved numerous adaptive responses to import the essential metals from the environment while preventing their excessive intracellular accumulation and intoxication (Chandrangsu et al, 2017). Cells often use high affinity transporters to import the metals with specificity and rely on specialized proteins and chaperones to integrate them into pathways dedicated to the synthesis of metalloproteins and enzyme cofactors (Buccella et al, 2019). Cobalt Resistance in Geobacter (Buccella et al, 2019) Each of these metals must be available in just the right intracellular concentration (i.e., the cellular metal quota) to prevent intoxication (Outten and O’Halloran, 2001). CoII intoxication causes generalized damage in the cells, requiring extensive reprogramming to cope with multiple stressors
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