Abstract
There have been considerable attempts in the past to relate phenotypic trait—habitat temperature of organisms—to their genotypes, most importantly compositions of their genomes and proteomes. However, despite accumulation of anecdotal evidence, an exact and conclusive relationship between the former and the latter has been elusive. We present an exhaustive study of the relationship between amino acid composition of proteomes, nucleotide composition of DNA, and optimal growth temperature (OGT) of prokaryotes. Based on 204 complete proteomes of archaea and bacteria spanning the temperature range from −10 °C to 110 °C, we performed an exhaustive enumeration of all possible sets of amino acids and found a set of amino acids whose total fraction in a proteome is correlated, to a remarkable extent, with the OGT. The universal set is Ile, Val, Tyr, Trp, Arg, Glu, Leu (IVYWREL), and the correlation coefficient is as high as 0.93. We also found that the G + C content in 204 complete genomes does not exhibit a significant correlation with OGT (R = −0.10). On the other hand, the fraction of A + G in coding DNA is correlated with temperature, to a considerable extent, due to codon patterns of IVYWREL amino acids. Further, we found strong and independent correlation between OGT and the frequency with which pairs of A and G nucleotides appear as nearest neighbors in genome sequences. This adaptation is achieved via codon bias. These findings present a direct link between principles of proteins structure and stability and evolutionary mechanisms of thermophylic adaptation. On the nucleotide level, the analysis provides an example of how nature utilizes codon bias for evolutionary adaptation to extreme conditions. Together these results provide a complete picture of how compositions of proteomes and genomes in prokaryotes adjust to the extreme conditions of the environment.
Highlights
As proteins and nucleic acids must remain in their native conformations at physiologically relevant temperatures, thermal adaptation requires adjustment of interactions within these biopolymers
E-mail: eugene@belok.harvard. edu Prokaryotes living at extreme environmental temperatures exhibit pronounced signatures in the amino acid composition of their proteins and the nucleotide compositions of their genomes, reflective of adaptation to their thermal environments
We performed a comprehensive analysis of amino acid and nucleotide compositional signatures of thermophylic adaptation by exhaustively evaluating all combinations of amino acids and nucleotides as possible determinants of optimal growth temperature (OGT) for all prokaryotic organisms with fully sequenced genomes
Summary
As proteins and nucleic acids must remain in their native conformations at physiologically relevant temperatures, thermal adaptation requires adjustment of interactions within these biopolymers. Given the limited alphabet of amino acid residues, an apparent way to control protein stability is to properly choose the fractions of different residue types and to arrange them in sequences that fold into stable and unique native structures [1,2,3,4] at physiological conditions of a given organism. Various mechanisms of thermostability were discussed in the literature, and many authors pointed to changes in amino acid composition as one of the clearest manifestations of thermal adaptation [2,4,5,6,7,8]. An early attempt of a systematic search for amino acids that are most significant for protein thermostability was made by Ponnuswamy et al [17], who considered a set of 30 proteins and about 65,000 combinations of different amino acids to find the amino acid sets serving as best predictors of denaturation temperature
Sign-in/Register to view highlights & summary Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
