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The GC Content as a Main Factor Shaping the Amino Acid Usage During Bacterial Evolution Process.

ABSTRACT: Understanding how proteins evolve is important, and the order of amino acids being recruited into the genetic codons was found to be an important factor shaping the amino acid composition of proteins. The latest work about the last universal common ancestor (LUCA) makes it possible to determine the potential factors shaping amino acid compositions during evolution. Those LUCA genes/proteins from Methanococcus maripaludis S2, which is one of the possible LUCA, were investigated. The evolutionary rates of these genes positively correlate with GC contents with P-value significantly lower than 0.05 for 94% homologous genes. Linear regression results showed that compositions of amino acids coded by GC-rich codons positively contribute to the evolutionary rates, while these amino acids tend to be gained in GC-rich organisms according to our results. The first principal component correlates with the GC content very well. The ratios of amino acids of the LUCA proteins coded by GC rich codons positively correlate with the GC content of different bacteria genomes, while the ratios of amino acids coded by AT rich codons negatively correlate with the increase of GC content of genomes. Next, we found that the recruitment order does correlate with the amino acid compositions, but gain and loss in codons showed newly recruited amino acids are not significantly increased along with the evolution. Thus, we conclude that GC content is a primary factor shaping amino acid compositions. GC content shapes amino acid composition to trade off the cost of amino acids with bases, which could be caused by the energy efficiency.

SUBMITTER: Du MZ

PROVIDER: S-EPMC6292993 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The characterization of functional elements in genomes relies on the identification of the footprints of natural selection. In this quest, taking into account neutral evolutionary processes such as mutation and genetic drift is crucial because these forces can generate patterns that may obscure or mimic signatures of selection. In mammals, and probably in many eukaryotes, another such confounding factor called GC-Biased Gene Conversion (gBGC) has been documented. This mechanism generates patterns identical to what is expected under selection for higher GC-content, specifically in highly recombining genomic regions. Recent results have suggested that a mysterious selective force favouring higher GC-content exists in Bacteria but the possibility that it could be gBGC has been excluded. Here, we show that gBGC is probably at work in most if not all bacterial species. First we find a consistent positive relationship between the GC-content of a gene and evidence of intra-genic recombination throughout a broad spectrum of bacterial clades. Second, we show that the evolutionary force responsible for this pattern is acting independently from selection on codon usage, and could potentially interfere with selection in favor of optimal AU-ending codons. A comparison with data from human populations shows that the intensity of gBGC in Bacteria is comparable to what has been reported in mammals. We propose that gBGC is not restricted to sexual Eukaryotes but also widespread among Bacteria and could therefore be an ancestral feature of cellular organisms. We argue that if gBGC occurs in bacteria, it can account for previously unexplained observations, such as the apparent non-equilibrium of base substitution patterns and the heterogeneity of gene composition within bacterial genomes. Because gBGC produces patterns similar to positive selection, it is essential to take this process into account when studying the evolutionary forces at work in bacterial genomes.

Project description:Bacterial evolution is characterized by strong purifying selection as well as rapid adaptive evolution in changing environments. In this context, the genomic GC content (genomic GC) varies greatly but presents some level of phylogenetic stability, making it challenging to explain based on current hypotheses. To illuminate the evolutionary mechanisms of the genomic GC, we analyzed the base composition and functional inventory of 11,083 representative genomes. A phylogenetically constrained bimodal distribution of the genomic GC, which mainly originated from parallel divergences in the early evolution, was demonstrated. Such variation of the genomic GC can be well explained by DNA replication and repair (DRR), in which multiple pathways correlate with the genomic GC. Furthermore, the biased conservation of various stress-related genes, especially the DRR-related ones, implies distinct adaptive processes in the ancestral lineages of high- or low-GC clades which are likely induced by major environmental changes. Our findings support that the mutational biases resulting from these legacies of ancient adaptation have changed the course of adaptive evolution and generated great variation in the genomic GC. This highlights the importance of indirect effects of natural selection, which indicates a new model for bacterial evolution. IMPORTANCE GC content has been shown to be an important factor in microbial ecology and evolution, and the genomic GC of bacteria can be characterized by great intergenomic heterogeneity, high intragenomic homogeneity, and strong phylogenetic inertia, as well as being associated with the environment. Current hypotheses concerning direct selection or mutational biases cannot well explain these features simultaneously. Our findings of the genomic GC showing that ancient adaptations have transformed the DRR system and that the resulting mutational biases further contributed to a bimodal distribution of it offer a more reasonable scenario for the mechanism. This would imply that, when thinking about the evolution of life, diverse processes of adaptation exist, and combined effects of natural selection should be considered.

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The GC Content as a Main Factor Shaping the Amino Acid Usage During Bacterial Evolution Process.

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