Adaptive role of increased frequency of polypurine tracts in mRNA sequences of thermophilic prokaryotes

Abstract

The mechanism of an organism's adaptation to high temperatures has been investigated intensively in recent years. It was suggested that the macromolecules of thermophilic microorganisms (especially proteins) have structural features that enhance their thermostability. We compared mRNA sequences of 72 fully sequenced prokaryotic proteomes (14 thermophilic and 58 mesophilic species). Although the differences between the percentage of adenine plus guanine content of whole mRNAs of different prokaryotic species are much lower than those of guanine plus cytosine content, the thermophile purinepyrimidine (R/Y) ratio within their mRNAs is significantly higher than that of the mesophiles. The first and third codon positions of both thermophiles and mesophiles are purine-biased, with the bias more pronounced by the thermophiles. Thermophile mRNAs that display the highest R/Y ratio (1.43-1.69) are those of the ribosomal proteins, histone-like proteins, DNA-dependent RNA polymerase subunits, and heat-shock proteins. Within mesophilic prokaryotes and five eukaryotic species, the R/Y ratio of the mRNAs of heat-shock proteins is higher than their average over coding part of the genome. Polypurine tracts (R) n (with n > 5) are much more abundant within the thermophile mRNAs compared with mesophiles. Between two sequential pure-purinic codons of thermophile mRNAs, there is a rather strong tendency for the occurrence of adenine but not guanine tracts. The data suggest that mixed adenine⅐guanine and polyadenine tracts in mRNAs increase the thermostability beyond the contribution of amino acids encoded by purine tracts, which highlights the importance of ecological stress in the evolution of genome architecture.A daptive strategies of organisms to extreme environments such as exceptional salinity, high pressure, nonphysiological pH, anaerobic conditions, and high and low temperatures are of primary importance for evolutionary studies (1). Revealing and understanding the special features of the macromolecules of thermophilic prokaryotes with high to very high optimum growth temperatures (OGTs) (50-113°C), compared with much lower ranges (20-37°C) of prokaryotic mesophiles, is of particular interest. Historically, investigators first were interested in revealing the unique features of the thermophile proteins that contribute to their thermostability (2, 3). Clarifying the principles of enhanced thermostability is important theoretically and practically. Deciphering improved enzymes with higher thermostability is of significant economic value to some industries. In this study, our aim was to unravel differences between mRNAs and the proteins of thermophiles and mesophiles to identify common features of the thermophiles' molecules that might contribute to thermostability. We restricted this study to the protein-coding transcripts. Understanding how the adaptation of the transcription and translation machinery (and products) to high temperature is achieved is central to both theoretical models and in vitro experimentation. Therefore, b...

Nucleotide Composition and Amino Acid Usage in AT-Rich Hyperthermophilic Species

“…The long standing hypothesis is that GC-richness of protein coding genes can not be considered as thermophilic signatures [17]. The above results confirm the findings of Paz et al [13] who reported abundance of polypurine tracts in thermophilic mRNA sequences, as purine loading of mRNAs is expected to reduce RNA-RNA interactions and thus prevent formation of double stranded RNA molecules [18]. Subsequently, frequency of each nucleotide for each of the three codon positions is analyzed.…”

“…Although considerable studies have focused on understanding the mechanisms that makes life possible under these conditions, it still remains unclear that whether it is due to external conditions or natural selection [4,7,[11][12][13][14]. In order to infer the molecular mechanistic adjustments to the thermal stress, it is desired to compare the genomic characteristics of hyperthermophiles with mesophilic genera.…”

Differences in dinucleotide frequencies of thermophilic genes encoding water soluble and membrane proteins

“…Kawashima et al (2000) reported that in archaea a simple combination of purine (R) and pyrimidine (Y) dinucleotides, RR+YY-RY-YR, is linearly correlated with optimal growth temperature (OGT). An increased frequency of purine nucleotides in the coding strands contributes to thermostability (Paz et al, 2004). It has been reported that a simple summation of the purines adenine and guanine (A+G) is correlated with OGT (Lambros et al, 2003;Zeldovich et al, 2007).…”

Classification and regression tree (CART) analyses of genomic signatures reveal sets of tetramers that discriminate temperature optima of archaea and bacteria

“…As noted by other authors (e.g. Lao and Forsdyke 2000, Lambros et al 2003, and Paz et al 2004, the coding regions of many thermophilic genomes are purineloaded and possess codon biases that reflect that loading. Our method of using a "virtual coding strand" eliminated the variable of gene orientation.…”