Energetic evolution of cellular Transportomes

Abstract

Background: Transporter proteins mediate the translocation of substances across the membranes of living cells. Many transport processes are energetically expensive and the cells use 20 to 60% of their energy to power the transportomes. We hypothesized that there may be an evolutionary selection pressure for lower energy transporters.

Results: We performed a genome-wide analysis of the compositional reshaping of the transportomes across the kingdoms of bacteria, archaea, and eukarya. We found that the share of ABC transporters is much higher in bacteria and archaea (ca. 27% of the transportome) than in primitive eukaryotes (13%), algae and plants (10%) and in fungi and animals (5-6%). This decrease is compensated by an increased occurrence of secondary transporters and ion channels. The share of ion channels is particularly high in animals (ca. 30% of the transportome) and algae and plants with (ca. 13%), when compared to bacteria and archaea with only 6-7%. Therefore, our results show a move to a preference for the low-energy-demanding transporters (ion channels and carriers) over the more energy-costly transporter classes (ATP-dependent families, and ABCs in particular) as part of the transition from prokaryotes to eukaryotes. The transportome analysis also indicated seven bacterial species, including Neorickettsia risticii and Neorickettsia sennetsu, as likely origins of the mitochondrion in eukaryotes, based on the phylogenetically restricted presence therein of clear homologues of modern mitochondrial solute carriers.

Conclusions: The results indicate that the transportomes of eukaryotes evolved strongly towards a higher energetic efficiency, as ATP-dependent transporters diminished and secondary transporters and ion channels proliferated. These changes have likely been important in the development of tissues performing energetically costly cellular functions.

Keywords: Cellular membrane; Energetic efficiency; Evolution; Mitochondria; Transporters.

Fig. 1

Transportomes differ in size among species and evolutionarily distant domains of life. (a) The number of membrane transporters per organism in relation to the genome size. (b) The number of membrane transporters per genome in relation to the number of total genes. (c) Percentage of transporter-coding genes in relation to gene density

Fig. 2

The evolutionary dynamics of transportomes composition. (a) Heat-map representation of the changes in the number of members of the transporter classes. To calculate the intra-genomic frequencies, the numbers of transporter members are normalized to the total number of genes per genome. The heat-map is drawn for each class of ion channels, secondary transporters, and ATP-dependent transporters and therefore colors are not comparable between the classes. (b) The fraction of ATP-dependent transporters in the transportomes. All of the variations of ATP-dependent transporters and ABC superfamily except the difference between bacteria and archaea are significant with a p-value less than 0.001. (c) The fraction of secondary transporters in the transportomes. Only the difference between bacteria and animals is not statistically significant (p = 0.635). (d) The fraction of ion channels in the transportomes. All differences, except among fungi, bacteria and archaea, are significant with a p-value less than 0.001. The values on panels b-d are shown as mean +/− t-test based 99% confidence intervals. The variations were also confirmed on the arc sin √x transformed data (See Additional file 2: Data S1). The family names of the transporters can also be found in the Additional file 2: Data S1

Fig. 3

The compositional changes in the transportomes of prokaryotes with different genome sizes. (a) Comparison between the transportome size and total gene number among prokaryotes including bacteria and archaea. All of the 126 studied species are clustered into three groups based on the total number of the genes. (b) The fraction of ATP-dependent transporters in the transportomes. (c) The fraction of secondary transporters in the transportomes. (d) The fraction of ion channels in the transportomes. The values on panels b-d are shown as mean +/− t-test based 99% confidence interval. The variations were also confirmed on the arc sin √x transformed data (See Additional file 2: Data S1). Group I and III differ significantly for all of the transporter classes with a p-value of < 0.001

Fig. 4

Number of transporter families that are shared between or are specific for prokaryotes and eukaryotes