Selection-driven cost-efficiency optimization of transcripts modulates gene evolutionary rate in bacteria.

BACKGROUND: Most amino acids are encoded by multiple synonymous codons. However, synonymous codons are not used equally, and this biased codon use varies between different organisms. It has previously been shown that both selection acting to increase codon translational efficiency and selection acting to decrease codon biosynthetic cost contribute to differences in codon bias. However, it is unknown how these two factors interact or how they affect molecular sequence evolution. RESULTS: Through analysis of 1320 bacterial genomes, we show that bacterial genes are subject to multi-objective selection-driven optimization of codon use. Here, selection acts to simultaneously decrease transcript biosynthetic cost and increase transcript translational efficiency, with highly expressed genes under the greatest selection. This optimization is not simply a consequence of the more translationally efficient codons being less expensive to synthesize. Instead, we show that transfer RNA gene copy number alters the cost-efficiency trade-off of synonymous codons such that, for many species, selection acting on transcript biosynthetic cost and translational efficiency act in opposition. Finally, we show that genes highly optimized to reduce cost and increase efficiency show reduced rates of synonymous and non-synonymous mutation. CONCLUSIONS: This analysis provides a simple mechanistic explanation for variation in evolutionary rate between genes that depends on selection-driven cost-efficiency optimization of the transcript. These findings reveal how optimization of resource allocation to messenger RNA synthesis is a critical factor that determines both the evolution and composition of genes.

Antisense transcription-dependent chromatin signature modulates sense transcript dynamics.

Antisense transcription is widespread in genomes. Despite large differences in gene size and architecture, we find that yeast and human genes share a unique, antisense transcription-associated chromatin signature. We asked whether this signature is related to a biological function for antisense transcription. Using quantitative RNA-FISH, we observed changes in sense transcript distributions in nuclei and cytoplasm as antisense transcript levels were altered. To determine the mechanistic differences underlying these distributions, we developed a mathematical framework describing transcription from initiation to transcript degradation. At GAL1, high levels of antisense transcription alter sense transcription dynamics, reducing rates of transcript production and processing, while increasing transcript stability. This relationship with transcript stability is also observed as a genome-wide association. Establishing the antisense transcription-associated chromatin signature through disruption of the Set3C histone deacetylase activity is sufficient to similarly change these rates even in the absence of antisense transcription. Thus, antisense transcription alters sense transcription dynamics in a chromatin-dependent manner.

Description of Phytomonas oxycareni n. sp. from the Salivary Glands of Oxycarenus lavaterae.

Phytomonas spp. (phytomonads) are a diverse and globally distributed group of unicellular eukaryotes that parasitize a wide range of plants and are transmitted by insect hosts. Here we report the discovery and characterisation of a new species of Phytomonas, named Phytomonas oxycareni n. sp., which was obtained from the salivary glands of the invasive species of true bug Oxycarenus lavaterae (Heteroptera). The new Phytomonas species exhibits a long slender promastigote morphology and can be found both within the lumen of the insect host's salivary glands as well as within the cells of the salivary gland itself. Sampling multiple individuals from the same population post-winter hibernation on two consecutive years revealed that infection was persistent over time. Finally, phylogenetic analyses of small subunit ribosomal RNA genes revealed that this species is sister to other species within the genus Phytomonas, providing new insight into the evolutionary history of the clade.

Dietary nitrogen alters codon bias and genome composition in parasitic microorganisms.

BACKGROUND: Genomes are composed of long strings of nucleotide monomers (A, C, G and T) that are either scavenged from the organism's environment or built from metabolic precursors. The biosynthesis of each nucleotide differs in atomic requirements with different nucleotides requiring different quantities of nitrogen atoms. However, the impact of the relative availability of dietary nitrogen on genome composition and codon bias is poorly understood. RESULTS: Here we show that differential nitrogen availability, due to differences in environment and dietary inputs, is a major determinant of genome nucleotide composition and synonymous codon use in both bacterial and eukaryotic microorganisms. Specifically, low nitrogen availability species use nucleotides that require fewer nitrogen atoms to encode the same genes compared to high nitrogen availability species. Furthermore, we provide a novel selection-mutation framework for the evaluation of the impact of metabolism on gene sequence evolution and show that it is possible to predict the metabolic inputs of related organisms from an analysis of the raw nucleotide sequence of their genes. CONCLUSIONS: Taken together, these results reveal a previously hidden relationship between cellular metabolism and genome evolution and provide new insight into how genome sequence evolution can be influenced by adaptation to different diets and environments.