Transmembrane Protein Oxygen Content and Compartmentalization of Cells

PLOS ONE, Jul 2008

Recently, there was a report that explored the oxygen content of transmembrane proteins over macroevolutionary time scales where the authors observed a correlation between the geological time of appearance of compartmentalized cells with atmospheric oxygen concentration. The authors predicted, characterized and correlated the differences in the structure and composition of transmembrane proteins from the three kingdoms of life with atmospheric oxygen concentrations in geological timescale. They hypothesized that transmembrane proteins in ancient taxa were selectively excluding oxygen and as this constraint relaxed over time with increase in the levels of atmospheric oxygen the size and number of communication-related transmembrane proteins increased. In summary, they concluded that compartmentalized and non-compartmentalized cells can be distinguished by how oxygen is partitioned at the proteome level. They derived this conclusion from an analysis of 19 taxa. We extended their analysis on a larger sample of taxa comprising 309 eubacterial, 34 archaeal, and 30 eukaryotic complete proteomes and observed that one can not absolutely separate the two groups of cells based on partition of oxygen in their membrane proteins. In addition, the origin of compartmentalized cells is likely to have been driven by an innovation than happened 2700 million years ago in the membrane composition of cells that led to the evolution of endocytosis and exocytosis rather than due to the rise in concentration of atmospheric oxygen.

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Transmembrane Protein Oxygen Content and Compartmentalization of Cells

Citation: Sasidharan R, Smith A, Gerstein M ( Transmembrane Protein Oxygen Content and Compartmentalization of Cells Rajkumar Sasidharan 0 Andrew Smith 0 Mark Gerstein 0 Berend Snel, Utrecht University, Netherlands 0 1 Molecular Biophysics and Biochemistry Department, Yale University , New Haven , Connecticut, United States of America, 2 Department of Computer Science, Yale University , New Haven , Connecticut, United States of America, 3 Interdepartmental Program in Computational Biology and Bioinformatics, Yale University , New Haven, Connecticut , United States of America Recently, there was a report that explored the oxygen content of transmembrane proteins over macroevolutionary time scales where the authors observed a correlation between the geological time of appearance of compartmentalized cells with atmospheric oxygen concentration. The authors predicted, characterized and correlated the differences in the structure and composition of transmembrane proteins from the three kingdoms of life with atmospheric oxygen concentrations in geological timescale. They hypothesized that transmembrane proteins in ancient taxa were selectively excluding oxygen and as this constraint relaxed over time with increase in the levels of atmospheric oxygen the size and number of communication-related transmembrane proteins increased. In summary, they concluded that compartmentalized and noncompartmentalized cells can be distinguished by how oxygen is partitioned at the proteome level. They derived this conclusion from an analysis of 19 taxa. We extended their analysis on a larger sample of taxa comprising 309 eubacterial, 34 archaeal, and 30 eukaryotic complete proteomes and observed that one can not absolutely separate the two groups of cells based on partition of oxygen in their membrane proteins. In addition, the origin of compartmentalized cells is likely to have been driven by an innovation than happened 2700 million years ago in the membrane composition of cells that led to the evolution of endocytosis and exocytosis rather than due to the rise in concentration of atmospheric oxygen. - . These authors contributed equally to this work. The evolution of multicellular forms of life represents a major transition in the evolution of complex organisms. Cellular compartmentalization was a natural consequence of this evolutionary shift that lead to a large-scale innovation in the origin of protein domains with roles in cellular communication. However, the events that led to this shift are not clear. On a sample size of 19 proteomes that comprised 6 eukaryotes, 9 eubacteria and 4 archaea, Acquisti et al. observed a correlation between the time of appearance of cellular compartmentalization and atmospheric oxygen concentration[1]. They propose that atmospheric oxygen levels influenced the composition of transmembrane proteins, and that older taxa (bacteria and archaea) exclude oxygen from lowoxygen transmembrane proteins to a greater extent than do younger taxa. They suggest that this constraint relaxed over time when atmospheric oxygen concentrations rose and led to the increase in size and number of receptors. They hypothesized that atmospheric oxygen concentrations affected the timing of evolution of cellular compartmentalization by constraining the size of domains necessary for cellular communication. Results and Discussion To support their claims the authors calculate the ratio of the number of low-oxygen transmembrane proteins to the number of high-oxygen ones for these 19 proteomes (Figure 5a on Page 50 of their article) and suggest that single-celled compartmentalized organisms, namely Saccharomyces cerevisiae, Giardia lamblia (unicellular eukaryotes), and Rhodopirellula baltica (planctomycete bacteria), are similar to eukaryotes in the proportion of their proteome that are high-oxygen transmembrane proteins. Eubacteria and archaea are similar in this respect and the authors infer from this that there is no systematic association between eukaryotic complexity, proteome oxygen partitioning, and atmospheric oxygen levels. They claimed this boils down to a basic functional difference associated with proteome composition and state that, of the 19 taxa, the only two groups that can be distinguished by how oxygen is partitioned at the proteome level are compartmentalized and non-compartmentalized cells. In our work, we reproduced this figure on a larger sample of complete proteomes (309 eubacteria, 34 archaea, and 30 eukaryote) available from NCBIs ftp site[2] (Figure 1a) using the same methods that authors used to derive their results. We observed that ,13% of the prokaryotic proteomes (40 eubacteria and 4 archaea excluding multiple strains) exhibit a ratio that is less than the highest ratio of 0.76 observed for a eukaryote (Bos Taurus). About 50% of the eukaryotes overlap with the range that we observed for prokaryotes. While there is a trend for lower ratios in eukaryotic proteomes, our data indicate that one c (...truncated)


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Rajkumar Sasidharan, Andrew Smith, Mark Gerstein. Transmembrane Protein Oxygen Content and Compartmentalization of Cells, PLOS ONE, 2008, 7, DOI: 10.1371/journal.pone.0002726