The biological chemistry of the transition metal “transportome” of Cupriavidus metallidurans

Abstract

This review tries to illuminate how the bacterium Cupriavidus metallidurans CH34 is able to allocate essential transition metal cations to their target proteins although these metals have similar charge-to-surface ratios and chemical features, exert toxic effects, compete with each other, and occur in the bacterial environment over a huge range of concentrations and speciations. Central to this ability is the "transportome", the totality of all interacting metal import and export systems, which, as an emergent feature, transforms the environmental metal content and speciation into the cellular metal mélange. In a kinetic flow equilibrium resulting from controlled uptake and efflux reactions, the periplasmic and cytoplasmic metal content is adjusted in a way that minimizes toxic effects. A central core function of the transportome is to shape the metal ion composition using high-rate and low-specificity reactions to avoid time and/or energy-requiring metal discrimination reactions. This core is augmented by metal-specific channels that may even deliver metals all the way from outside of the cell to the cytoplasm. This review begins with a description of the basic chemical features of transition metal cations and the biochemical consequences of these attributes, and which transition metals are available to C. metallidurans. It then illustrates how the environment influences the metal content and speciation, and how the transportome adjusts this metal content. It concludes with an outlook on the fate of metals in the cytoplasm. By generalization, insights coming from C. metallidurans shed light on multiple transition metal homoeostatic mechanisms in all kinds of bacteria including pathogenic species, where the "battle" for metals is an important part of the host-pathogen interaction.

Synergistic Toxicity of Copper and Gold Compounds in Cupriavidus metallidurans

“…The weathering of many transition metal-containing minerals releases H 2 , which is an attractive energy source for this facultative lithotrophic bacterium, making aurifer-ous soils and minerals an interesting environment for the C. metallidurans. Here, abundant energy is present, and competition by organisms without sophisticated metal detoxification systems is limited (1,6,(25)(26)(27)(28). However, synergistic Cu and Au toxicity is an important threat for C. metallidurans in auriferous environments, and we identified the molecular mechanism for this process.…”

Comparative Insights Into the Complete Genome Sequence of Highly Metal Resistant Cupriavidus metallidurans Strain BS1 Isolated From a Gold–Copper Mine

“…In order to maintain metal homeostasis in the presence of multiple heavy metals, the transportome contains the metal uptake systems in addition to the metal efflux systems as the first pillar of defense (Nies, 2016). The strain BS1 shows a high degree of conservation on gene and amino acid sequence level as well as the gene loci synteny of the metal uptake systems encoding genome regions in comparison to strain CH34.…”

“…Instead of the missing sigma factor, strain BS1 harbors one additional (SigX) with 74.5% similarity on amino acid level to RpoO ( Supplementary Table S2). This metallophilic strain BS1, harbors numerous gene clusters encoding metal-resistance determinants enabling detoxification of transition metal ions and complexes (Nies, 2003(Nies, , 2016. With regard to synteny and genome plasticity, mediated by mobile elements, C. metallidurans strain BS1 displayed a transfer of the metal resistance super cluster I from plasmid (pMOL30 in CH34) to chromid ( Supplementary Table S4 and Figures 6, 7).…”

Metal Selectivity of a Cd-, Co-, and Zn-Transporting P1B-type ATPase

“…29 The ability of C. metallidurans to survive in such metal-polluted conditions derives from the plethora of metal-resistance proteins that are encoded chromosomally or on two endogenous megaplasmids, pMOL28 and pMOL30. 30,31 In addition to several resistance-nodulation-division (RND)-driven and cation diffusion facilitator (CDF) efflux systems, C. metallidurans possesses genes for eight P 1B -ATPases. 26,31 Four are P 1B-1 -ATPases likely responsible for Cu + transport, three are P 1B-2 -ATPases likely responsible for Zn 2+ /Cd 2+ /Pb 2+ transport, 31–33 and the final is a distinct P 1B-4 -ATPase that is part of the larger gene cluster czc (cobalt, zinc, and cadmium resistance system) and is known as CzcP.…”