Abstract
Copper is an essential transition metal whose redox properties are used for a variety of enzymatic oxido-reductions and in electron transfer chains. It is also toxic to living beings, and therefore its cellular concentration must be strictly controlled. We have performed in silico analyses of the predicted proteomes of more than one hundred species of β proteobacteria to characterize their copper-related proteomes, including cuproproteins, i.e., proteins with active-site copper ions, copper chaperones, and copper-homeostasis systems. Copper-related proteomes represent between 0 and 1.48% of the total proteomes of β proteobacteria. The numbers of cuproproteins are globally proportional to the proteome sizes in all phylogenetic groups and strongly linked to aerobic respiration. In contrast, environmental bacteria have considerably larger proportions of copper-homeostasis systems than the other groups of bacteria, irrespective of their proteome sizes. Evolution toward commensalism, obligate, host-restricted pathogenesis or symbiosis is globally reflected in the loss of copper-homeostasis systems. In endosymbionts, defense systems and copper chaperones have disappeared, whereas residual cuproenzymes are electron transfer proteins for aerobic respiration. Lifestyle is thus a major determinant of the size and composition of the copper-related proteome, and it is particularly reflected in systems involved in copper homeostasis. Analyses of the copper-related proteomes of a number of species belonging to the Burkholderia, Bordetella, and Neisseria genera indicates that commensals are in the process of shedding their copper-homeostasis systems and chaperones to greater extents yet than pathogens.
Highlights
Β proteobacteria form a large phylogenetic group mainly composed of environmental species and a few important pathogens, notably of the Burkholderia, Bordetella, and Neisseria genera. β proteobacteria comprise a few known phytopathogens, commensals, endophytes, symbionts, and endosymbionts
Β proteobacteria include Cupriavidus metallidurans, aptly named from its capacity to survive in environments heavily contaminated with transition metals, as it was first isolated from the sludge of a decantation tank in a zinc factory (Mergeay et al, 1985)
As our results have indicated that the copper homeostasis protein complements found in β proteobacteria appear to correlate with lifestyles better than cuproproteins or chaperones, we first used the homeostasis subset of copper-related proteins to perform hierarchical clustering
Summary
Β proteobacteria form a large phylogenetic group mainly composed of environmental species and a few important pathogens, notably of the Burkholderia, Bordetella, and Neisseria genera. β proteobacteria comprise a few known phytopathogens, commensals, endophytes, symbionts, and endosymbionts. Β proteobacteria include Cupriavidus metallidurans, aptly named from its capacity to survive in environments heavily contaminated with transition metals, as it was first isolated from the sludge of a decantation tank in a zinc factory (Mergeay et al, 1985) This organism is extremely well equipped to deal with excessive concentrations of those elements including copper, either by efflux, complexation or reducing precipitation (Von Rozycki and Nies, 2009; Grosse et al, 2016; Herzberg et al, 2016). Bordetella bronchiseptica, a close relative of B. pertussis with a larger genome and a more promiscuous lifestyle, that can survive in the environment in addition to infecting mammals (Taylor-Mulneix et al, 2017), has more copper-regulated defense systems against excess of this metal than B. pertussis (our unpublished observations) This finding prompted us to analyze the predicted copperrelated proteomes of a large range of β proteobacteria to investigate more broadly the links between their lifestyles and the homeostasis of this metal
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