Dataset Information

Selection for energy efficiency drives strand-biased gene distribution in prokaryotes.

ABSTRACT: Lagging-strand genes accumulate more deleterious mutations. Genes are thus preferably located on the leading strand, an observation known as strand-biased gene distribution (SGD). Despite of this mechanistic understanding, a satisfactory quantitative model is still lacking. Replication-transcription-collisions induce stalling of the replication machinery, expose DNA to various attacks, and are followed by error-prone repairs. We found that mutational biases in non-transcribed regions can explain ~71% of the variations in SGDs in 1,552 genomes, supporting the mutagenesis origin of SGD. Mutational biases introduce energetically cheaper nucleotides on the lagging strand, and result in more expensive protein products; consistently, the cost difference between the two strands explains ~50% of the variance in SGDs. Protein costs decrease with increasing gene expression. At similar expression levels, protein products of leading-strand genes are generally cheaper than lagging-strand genes; however, highly-expressed lagging genes are still cheaper than lowly-expressed leading genes. Selection for energy efficiency thus drives some genes to the leading strand, especially those highly expressed and essential, but certainly not all genes. Stronger mutational biases are often associated with low-GC genomes; as low-GC genes encode expensive proteins, low-GC genomes thus tend to have stronger SGDs to alleviate the stronger pressure on efficient energy usage.

SUBMITTER: Gao N

PROVIDER: S-EPMC5585166 | biostudies-literature | 2017 Sep

REPOSITORIES: biostudies-literature

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Selection for energy efficiency drives strand-biased gene distribution in prokaryotes.

Gao Na N Lu Guanting G Lercher Martin J MJ Chen Wei-Hua WH

Scientific reports 20170905 1

Lagging-strand genes accumulate more deleterious mutations. Genes are thus preferably located on the leading strand, an observation known as strand-biased gene distribution (SGD). Despite of this mechanistic understanding, a satisfactory quantitative model is still lacking. Replication-transcription-collisions induce stalling of the replication machinery, expose DNA to various attacks, and are followed by error-prone repairs. We found that mutational biases in non-transcribed regions can explain ...[more]

PMID: 28874819

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Project description:BACKGROUND: The Firmicutes often possess three conspicuous genome features: marked Purine Asymmetry (PAS) across two strands of replication, Strand-biased Gene Distribution (SGD) and presence of two isoforms of DNA polymerase III alpha subunit, PolC and DnaE. Despite considerable research efforts, it is not clear whether the co-existence of PAS, PolC and/or SGD is an essential and exclusive characteristic of the Firmicutes. The nature of correlations, if any, between these three features within and beyond the lineages of Firmicutes has also remained elusive. The present study has been designed to address these issues. RESULTS: A large-scale analysis of diverse bacterial genomes indicates that PAS, PolC and SGD are neither essential nor exclusive features of the Firmicutes. PolC prevails in four bacterial phyla: Firmicutes, Fusobacteria, Tenericutes and Thermotogae, while PAS occurs only in subsets of Firmicutes, Fusobacteria and Tenericutes. There are five major compositional trends in Firmicutes: (I) an explicit PAS or G?+?A-dominance along the entire leading strand (II) only G-dominance in the leading strand, (III) alternate stretches of purine-rich and pyrimidine-rich sequences, (IV) G?+?T dominance along the leading strand, and (V) no identifiable patterns in base usage. Presence of strong SGD has been observed not only in genomes having PAS, but also in genomes with G-dominance along their leading strands - an observation that defies the notion of co-occurrence of PAS and SGD in Firmicutes. The PolC-containing non-Firmicutes organisms often have alternate stretches of R-dominant and Y-dominant sequences along their genomes and most of them show relatively weak, but significant SGD. Firmicutes having G?+?A-dominance or G-dominance along LeS usually show distinct base usage patterns in three codon sites of genes. Probable molecular mechanisms that might have incurred such usage patterns have been proposed. CONCLUSION: Co-occurrence of PAS, strong SGD and PolC should not be regarded as a genome signature of the Firmicutes. Presence of PAS in a species may warrant PolC and strong SGD, but PolC and/or SGD not necessarily implies PAS.

Project description:Codon usage bias in prokaryotic genomes is largely a consequence of background substitution patterns in DNA, but highly expressed genes may show a preference towards codons that enable more efficient and/or accurate translation. We introduce a novel approach based on supervised machine learning that detects effects of translational selection on genes, while controlling for local variation in nucleotide substitution patterns represented as sequence composition of intergenic DNA. A cornerstone of our method is a Random Forest classifier that outperformed previous distance measure-based approaches, such as the codon adaptation index, in the task of discerning the (highly expressed) ribosomal protein genes by their codon frequencies. Unlike previous reports, we show evidence that translational selection in prokaryotes is practically universal: in 460 of 461 examined microbial genomes, we find that a subset of genes shows a higher codon usage similarity to the ribosomal proteins than would be expected from the local sequence composition. These genes constitute a substantial part of the genome--between 5% and 33%, depending on genome size--while also exhibiting higher experimentally measured mRNA abundances and tending toward codons that match tRNA anticodons by canonical base pairing. Certain gene functional categories are generally enriched with, or depleted of codon-optimized genes, the trends of enrichment/depletion being conserved between Archaea and Bacteria. Prominent exceptions from these trends might indicate genes with alternative physiological roles; we speculate on specific examples related to detoxication of oxygen radicals and ammonia and to possible misannotations of asparaginyl-tRNA synthetases. Since the presence of codon optimizations on genes is a valid proxy for expression levels in fully sequenced genomes, we provide an example of an "adaptome" by highlighting gene functions with expression levels elevated specifically in thermophilic Bacteria and Archaea.

Project description:Gene transfer agents (GTAs) are virus-like elements integrated into bacterial genomes, particularly, those of Alphaproteobacteria The GTAs can be induced under conditions of nutritional stress, incorporate random fragments of bacterial DNA into miniphage particles, lyse the host cells, and infect neighboring bacteria, thus enhancing horizontal gene transfer. We show that GTA genes evolve under conditions of pronounced positive selection for the reduction of the energy cost of protein production as shown by comparison of the amino acid compositions with those of both homologous viral genes and host genes. The energy saving in GTA genes is comparable to or even more pronounced than that in the genes encoding the most abundant, essential bacterial proteins. In cases in which viruses acquire genes from GTAs, the bias in amino acid composition disappears in the course of evolution, showing that reduction of the energy cost of protein production is an important factor of evolution of GTAs but not bacterial viruses. These findings strongly suggest that GTAs represent bacterial adaptations rather than selfish, virus-like elements. Because GTA production kills the host cell and does not propagate the GTA genome, it appears likely that the GTAs are retained in the course of evolution via kin or group selection. Therefore, we hypothesize that GTAs facilitate the survival of bacterial populations under energy-limiting conditions through the spread of metabolic and transport capabilities via horizontal gene transfer and increases in nutrient availability resulting from the altruistic suicide of GTA-producing cells.IMPORTANCE Kin selection and group selection remain controversial topics in evolutionary biology. We argue that these types of selection are likely to operate in bacterial populations by showing that bacterial gene transfer agents (GTAs), but not related viruses, evolve under conditions of positive selection for the reduction of the energy cost of GTA particle production. We hypothesize that GTAs are dedicated devices mediating the survival of bacteria under conditions of nutrient limitation. The benefits conferred by GTAs under nutritional stress conditions appear to include horizontal dissemination of genes that could provide bacteria with enhanced capabilities for nutrient utilization and increases of nutrient availability occurring through the lysis of GTA-producing bacteria.

Dataset Information

Selection for energy efficiency drives strand-biased gene distribution in prokaryotes.

Publications

Selection for energy efficiency drives strand-biased gene distribution in prokaryotes.

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