General trends in trace element utilization revealed by comparative genomic analyses of Co, Cu, Mo, Ni, and Se

Abstract

Trace elements are used by all organisms and provide proteins with unique coordination and catalytic and electron transfer properties. Although many trace element-containing proteins are well characterized, little is known about the general trends in trace element utilization. We carried out comparative genomic analyses of copper, molybdenum, nickel, cobalt (in the form of vitamin B(12)), and selenium (in the form of selenocysteine) in 747 sequenced organisms at the following levels: (i) transporters and transport-related proteins, (ii) cofactor biosynthesis traits, and (iii) trace element-dependent proteins. Few organisms were found to utilize all five trace elements, whereas many symbionts, parasites, and yeasts used only one or none of these elements. Investigation of metalloproteomes and selenoproteomes revealed examples of increased utilization of proteins that use copper in land plants, cobalt in Dehalococcoides and Dictyostelium, and selenium in fish and algae, whereas nematodes were found to have great diversity of copper transporters. These analyses also characterized trace element metabolism in common model organisms and suggested new model organisms for experimental studies of individual trace elements. Mismatches in the occurrence of user proteins and corresponding transport systems revealed deficiencies in our understanding of trace element biology. Biological interactions among some trace elements were observed; however, such links were limited, and trace elements generally had unique utilization patterns. Finally, environmental factors, such as oxygen requirement and habitat, correlated with the utilization of certain trace elements. These data provide insights into the general features of utilization and evolution of trace elements in the three domains of life.

FIGURE 1.

Overview of utilization of five trace elements in the three domains of life. The tree is based on a highly resolved tree of life, which was simplified to only show major branches. Phyla in which more than half of organisms use all five trace elements are shown in red (if having at least three organisms, shown in bold). Phyla in which no organisms use any of the five trace elements are shown in blue (if having at least three organisms, shown in bold). The length of the colored section of each bar represents a proportion of organisms that use the corresponding trace element among all sequenced organisms in this phylum. The number and percentage of organisms that utilize individual trace elements in each domain of life are also shown.

FIGURE 2.

Metalloproteomes and selenoproteomes in bacteria. This figure shows the numbers of proteins that use the indicated trace elements in each sequenced bacterium. Organisms containing the largest eukaryotic metalloproteomes (for Cu, Mo, Ni, and Co) and selenoproteomes are indicated. Phyla in which the majority of sequenced organisms use all five trace elements are highlighted in red.

FIGURE 3.

Metalloproteomes and selenoproteomes in archaea. This figure shows the numbers of proteins that use indicated trace elements in each sequenced archaeon. Organisms containing the largest metalloproteomes (for Cu, Mo, Ni, and Co) and selenoproteome are indicated. Phyla in which the majority of sequenced organisms use all five trace elements are highlighted in red. Phyla in which none of the sequenced organisms use any of the five trace elements are shown in blue.

FIGURE 4.

Metalloproteomes and selenoproteomes in eukaryotes. This figure shows the numbers of proteins that use indicated trace elements in each sequenced eukaryote. Organisms with the largest metalloproteomes (Cu, Mo, Ni, and Co) and selenoproteomes are indicated. Phyla in which the majority of sequenced organisms use all five trace elements are highlighted in red. Phyla in which none of the sequenced organisms use any of the five trace elements are shown in blue.

FIGURE 5.

Multiple alignment of CusB proteins and other membrane fusion protein homologs. Positions of three methionines that are conserved in the N-terminal segment of CusB proteins are highlighted in red background. Other conserved residues are shown in white on black or gray.

FIGURE 6.

Relationship between environmental factors, classification of organisms, and trace element utilization traits in prokaryotes. A, oxygen requirement; B, different host-associated lifestyles.

FIGURE 7.

Relationship between parasitic lifestyles and trace element utilization traits in eukaryotes. P, parasites; NP, non-parasites. The majority of parasites lack the Mo, Ni, and Co utilization traits.