Relationships Between Copper-Related Proteomes and Lifestyles in β Proteobacteria

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.

Streamlined copper defenses make Bordetella pertussis reliant on custom-made operon

“…Loss of copper homeostasis systems in B. pertussis. Comparative genomic analyses revealed that the exclusively human pathogen B. pertussis and its close relative B. bronchiseptica share common sets of copper-homeostasis genes, including genes coding for a CopA ATPase, a PcoA-PcoB-type MCO system, and CopZ, CopI, and CusF copper chaperones, but both lack cusABC genes 18 . A copper storage protein (csp) gene is present in the B. bronchiseptica but not in the B. pertussis genome 18 .…”

“…Therefore, they have developed large resistance arsenals against copper intoxication. Conversely, bacteria with restricted ecological niches, such as pathogens or commensals, appear to have fewer copper homeostasis genes 18 . Here, we investigated copper homeostasis in the whooping cough agent Bordetella pertussis, a predominantly extracellular pathogen whose sole natural niche is the human upper respiratory tract 19 .…”

Cu Homeostasis in Bacteria: The Ins and Outs

“…The transcription of genes or operons involved in Cu export are generally activated when excess Cu is detected in the cytoplasm or periplasm. Transcriptional regulators of the MerR, ArsR, or CsoR families [ 6 , 252 , 290 ] sense Cu in the cytoplasm, while two-component systems such as CusRS or CopRS monitor the periplasmic Cu pool. The periplasmic and cytosolic Cu sensing systems can be independently activated, which probably allows for the prevention of Cu toxicity in the respective compartments [ 252 ].…”

“…Furthermore, human macrophages pump copper into their phagosomes after engulfing pathogenic bacteria to induce oxidative stress and bacterial cell death [ 4 ]. Consequently, bacteria have to deal with high copper concentrations in order to evade the host immune system [ 4 , 5 , 6 , 7 ]. The importance of Cu detoxifying systems for bacterial virulence is exemplified by the observation that the inactivation of Cu-exporting P 1B -type ATPases in Mycobacterium tuberculosis impairs their ability to proliferate in host macrophages [ 8 , 9 ].…”

Copper and Melanin Play a Role in Myxococcus xanthus Predation on Sinorhizobium meliloti

“…It has recently been reported that the bacterial lifestyle shapes their copper-related proteome, and this is particularly observed in systems involved in copper homeostasis (Antoine et al, 2019). The soil bacterium Cupriavidus necator, which is a predator extraordinarily resistant to copper, uses a toxic copper-binding peptide to kill the actinomycete Agromyces ramosus (Casida, 1987(Casida, , 1988, and its predatory activity against B. subtilis increases after exposure to copper in a concentrationdependent manner (Seccareccia et al, 2016).…”