Evolution of proteomes: fundamental signatures and global trends in amino acid compositions

Abstract

Background: The evolutionary characterization of species and lifestyles at global levels is nowadays a subject of considerable interest, particularly with the availability of many complete genomes. Are there specific properties associated with lifestyles and phylogenies? What are the underlying evolutionary trends? One of the simplest analyses to address such questions concerns characterization of proteomes at the amino acids composition level.

Results: In this work, amino acid compositions of a large set of 208 proteomes, with significant number of representatives from the three phylogenetic domains and different lifestyles are analyzed, resorting to an appropriate multidimensional method: Correspondence analysis. The analysis reveals striking discrimination between eukaryotes, prokaryotic mesophiles and hyperthemophiles-themophiles, following amino acid usage. In sharp contrast, no similar discrimination is observed for psychrophiles. The observed distributional properties are compared with various inferred chronologies for the recruitment of amino acids into the genetic code. Such comparisons reveal correlations between the observed segregations of species following amino acid usage, and the separation of amino acids following early or late recruitment.

Conclusion: A simple description of proteomes according to amino acid compositions reveals striking signatures, with sharp segregations or on the contrary non-discriminations following phylogenies and lifestyles. The distribution of species, following amino acid usage, exhibits a discrimination between [high GC]-[high optimal growth temperatures] and [low GC]-[moderate temperatures] characteristics. This discrimination appears to coincide closely with the separation of amino acids following their inferred early or late recruitment into the genetic code. Taken together the various results provide a consistent picture for the evolution of proteomes, in terms of amino acid usage.

Figure 1

Species distribution following amino-acid compositions. Factorial plane representation, with Correspondence analysis, for the distribution of species following amino acid compositions. Species names are reported whenever possible (for full list see Additional file 1). Amino acids (one letter) are represented in green. Coding colours for hyperthemophiles, thermophiles, prokaryotic mesophiles, psychrophiles and eukaryotes are following legend in Figure 1A. Three main groups, corresponding to hyperthermophiles-thermophiles; prokaryotic mesophiles-psychrophiles and eukaryotes are roughly delimited by horizontal dashed grey lines. A: Legend for colour coding symbols. Species and barycenters symbols for the various groups that are reported in Figures 1, 2, 3 and 4 with the same colour coding conventions.

Figure 2

Species distribution, physico-chemical signatures and proteins conservations. Factorial plane representation and species colour coding are as in Figure 1 (species are only reported with their positions; see legend for colour coding symbols in Figure 1A). Amino acids (one letter) are in green. The three pools for polar (POL), charged (CHAR) and hydrophobic (HYD) amino acids are reported in black. The positions of the subsets corresponding to specific proteins (SPEC), as well as to proteins exclusively conserved in one (E, A and B) or in combinations of phylogenetic domains (EA, EB, AB and EAB) are reported in pink.

Figure 3

Species distribution and characteristic amino-acid compositional signatures. Factorial plane representation and species colour coding are as in Figure 1. Amino acids (three letters) are discriminated according to statistically significant mean compositional differences (at the probability level of p < 0.001, see text and Additional file 3) between the three segregated groups (hyperthermophiles-thermophiles, HTH-TH; prokaryotic mesophiles-psychrophiles, PMES-PSYC; eukaryotes, EUK): amino acids in pale blue (Val, His, Ser) are characteristic for each of the three groups; amino acids in orange (Tyr, Glu, Asp, Thr, Gln) are characteristic for HTH-TH; amino acids in dark blue (Gly, Ile, Leu, Cys) are characteristic for EUK; amino acids in black (Lys, Asn, Phe, Met, Trp, Arg) show no significant differences between the three groups (Ala and Pro show only partial significant differences: between EUK and PMES-PSYC); for a given class, underlined amino acids correspond to high values steadily decreasing in the three groups downward (HTH-TH to PMES-PSYC and to EUK) whereas non-underlined amino acids correspond to low values steadily increasing in the same direction.

Figure 4

Amino acids distribution and chronological models for the recruitment into the genetic code. Factorial plane representation and species colour coding symbols are as in Figure 1. Dashed diagonal line in grey separates roughly the territory T1 ([high optimal growth temperature]-[high GC content]) from the territory T2 ([moderate optimal growth temperature]-[low GC content]), with arrow pointing from T1 to T2. Colour coding for amino-acids is following the model of Jordan et al. [9]: "strong losers" are orange (Glu, Gly, Ala, Pro); "weak loser" Lys is orange with a black outline; "strong gainers" are filled black (Cys, Ser, His, Phe, Met); "weak gainers" have black outlines (Asn, Ile, Thr, Val); all other amino acids are green. Amino acids found in Miller's experiments [14] or in the Murchison meteorite [15] are labelled with black, respectively red, crosses (the number of crosses, in each colour, follows the reported abundances for the corresponding amino acids; see Additional Table 3 in Jordan et al. [9]). Numbering of amino acids in blue is following the chronology compiled by Trifonov (Figure 1 in [10]; with possible different codon chronologies associated with a given amino acid, such as for Ser ranking 6 or 11 following the codon).