Dataset Information

Occurrence, evolution, and functions of DNA phosphorothioate epigenetics in bacteria.

ABSTRACT: The chemical diversity of physiological DNA modifications has expanded with the identification of phosphorothioate (PT) modification in which the nonbridging oxygen in the sugar-phosphate backbone of DNA is replaced by sulfur. Together with DndFGH as cognate restriction enzymes, DNA PT modification, which is catalyzed by the DndABCDE proteins, functions as a bacterial restriction-modification (R-M) system that protects cells against invading foreign DNA. However, the occurrence of dnd systems across a large number of bacterial genomes and their functions other than R-M are poorly understood. Here, a genomic survey revealed the prevalence of bacterial dnd systems: 1,349 bacterial dnd systems were observed to occur sporadically across diverse phylogenetic groups, and nearly half of these occur in the form of a solitary dndBCDE gene cluster that lacks the dndFGH restriction counterparts. A phylogenetic analysis of 734 complete PT R-M pairs revealed the coevolution of M and R components, despite the observation that several PT R-M pairs appeared to be assembled from M and R parts acquired from distantly related organisms. Concurrent epigenomic analysis, transcriptome analysis, and metabolome characterization showed that a solitary PT modification contributed to the overall cellular redox state, the loss of which perturbed the cellular redox balance and induced Pseudomonas fluorescens to reconfigure its metabolism to fend off oxidative stress. An in vitro transcriptional assay revealed altered transcriptional efficiency in the presence of PT DNA modification, implicating its function in epigenetic regulation. These data suggest the versatility of PT in addition to its involvement in R-M protection.

SUBMITTER: Tong T

PROVIDER: S-EPMC5879708 | biostudies-literature | 2018 Mar

REPOSITORIES: biostudies-literature

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Occurrence, evolution, and functions of DNA phosphorothioate epigenetics in bacteria.

Tong Tong T Chen Si S Wang Lianrong L Tang You Y Ryu Jae Yong JY Jiang Susu S Wu Xiaolin X Chen Chao C Luo Jie J Deng Zixin Z Li Zhiqiang Z Lee Sang Yup SY Chen Shi S

Proceedings of the National Academy of Sciences of the United States of America 20180312 13

The chemical diversity of physiological DNA modifications has expanded with the identification of phosphorothioate (PT) modification in which the nonbridging oxygen in the sugar-phosphate backbone of DNA is replaced by sulfur. Together with DndFGH as cognate restriction enzymes, DNA PT modification, which is catalyzed by the DndABCDE proteins, functions as a bacterial restriction-modification (R-M) system that protects cells against invading foreign DNA. However, the occurrence of <i>dnd</i> sys ...[more]

PMID: 29531068

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Project description:The prevailing theory for the molecular basis of evolution involves genetic mutations that ultimately generate the heritable phenotypic variation on which natural selection acts. However, epigenetic transgenerational inheritance of phenotypic variation may also play an important role in evolutionary change. A growing number of studies have demonstrated the presence of epigenetic inheritance in a variety of different organisms that can persist for hundreds of generations. The possibility that epigenetic changes can accumulate over longer periods of evolutionary time has seldom been tested empirically. This study was designed to compare epigenetic changes among several closely related species of Darwin's finches, a well-known example of adaptive radiation. Erythrocyte DNA was obtained from five species of sympatric Darwin's finches that vary in phylogenetic relatedness. Genome-wide alterations in genetic mutations using copy number variation (CNV) were compared with epigenetic alterations associated with differential DNA methylation regions (epimutations). Epimutations were more common than genetic CNV mutations among the five species; furthermore, the number of epimutations increased monotonically with phylogenetic distance. Interestingly, the number of genetic CNV mutations did not consistently increase with phylogenetic distance. The number, chromosomal locations, regional clustering, and lack of overlap of epimutations and genetic mutations suggest that epigenetic changes are distinct and that they correlate with the evolutionary history of Darwin's finches. The potential functional significance of the epimutations was explored by comparing their locations on the genome to the location of evolutionarily important genes and cellular pathways in birds. Specific epimutations were associated with genes related to the bone morphogenic protein, toll receptor, and melanogenesis signaling pathways. Species-specific epimutations were significantly overrepresented in these pathways. As environmental factors are known to result in heritable changes in the epigenome, it is possible that epigenetic changes contribute to the molecular basis of the evolution of Darwin's finches.

Project description:The prevailing theory for the molecular basis of evolution involves genetic mutations that ultimately generate the heritable phenotypic variation on which natural selection acts. However, epigenetic transgenerational inheritance of phenotypic variation may also play an important role in evolutionary change. A growing number of studies have demonstrated the presence of epigenetic inheritance in a variety of different organisms that can persist for hundreds of generations. The possibility that epigenetic changes could accumulate over macroevolutionary time has been considered, but not yet seldom been tested empirically. The current study was designed to compare epigenetic changes among several closely related species of Darwin’s finches, a well-known example of adaptive radiation. Erythrocyte DNA was obtained from five species of sympatric Darwin's finches that vary in phylogenetic relatedness. Genome wide alterations in genetic mutations using copy number variation (CNV) were compared to epigenetic alterations associated with differential DNA methylation regions (epimutations). Epimutations were more common than genetic CNV mutations among the five species; furthermore, the number of epimutations increased monotonically with phylogenetic distance. Interestingly, the number of genetic CNV mutations did not consistently increase with phylogenetic distance. The number, chromosomal locations, regional clustering, and lack of overlap of epimutations and genetic mutations suggests that epigenetic changes are distinct and that they correlate with the evolutionary history of Darwin’s finches. The potential functional significance of the epimutations was explored by comparing their locations on the genome to the location of evolutionarily important genes and cellular pathways in birds. Specific epimutations were associated with genes related to the bone morphogenic protein (BMP), toll receptor, and melanogenesis signaling pathways. Species- specific epimutations were significantly over-represented in these pathways. Since environmental factors are known to rapidly alter heritable changes in the epigenome, it is possible that epigenetic changes have played a contributing role in the molecular basis of the evolution of Darwin's finches.

Dataset Information

Occurrence, evolution, and functions of DNA phosphorothioate epigenetics in bacteria.

Publications

Occurrence, evolution, and functions of DNA phosphorothioate epigenetics in bacteria.

Similar Datasets

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