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.
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. 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)