Horizontal gene transfer barrier shapes the evolution of prokaryotic pangenomes

AbstractThe genomes of bacteria and archaea evolve by extensive loss and gain of genes which, for any group of related prokaryotic genomes, result in the formation of a pangenome with the universal, asymmetrical U-shaped distribution of gene commonality. To elucidate the evolutionary factors that define the specific shape of this distribution, we investigate the fit of simple models of genome evolution to the empirically observed gene commonality distributions and genomes intersections for 33 groups of closely related bacterial genomes. The combined analysis of genome intersections and gene commonality shows that at least one of the two simplifying assumptions that are usually adopted for modeling the evolution of the U-shaped distribution, those of infinitely many genes and constant genome size, is invalid. The violation of both these assumptions stems from the horizontal gene transfer barrier, i.e. the cost of accommodation of foreign genes by prokaryotes.

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Disentangling the effects of selection and loss bias on gene dynamics

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1704925114 ◽

2017 ◽

Vol 114 (28) ◽

pp. E5616-E5624 ◽

Cited By ~ 14

Author(s):

Jaime Iranzo ◽

José A. Cuesta ◽

Susanna Manrubia ◽

Mikhail I. Katsnelson ◽

Eugene V. Koonin

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Genome Size ◽

Loss Ratio ◽

Effective Population ◽

Selfish Behavior ◽

Fitness Effects ◽

Prokaryotic Genomes ◽

Functional Classes ◽

The Cost

We combine mathematical modeling of genome evolution with comparative analysis of prokaryotic genomes to estimate the relative contributions of selection and intrinsic loss bias to the evolution of different functional classes of genes and mobile genetic elements (MGE). An exact solution for the dynamics of gene family size was obtained under a linear duplication–transfer–loss model with selection. With the exception of genes involved in information processing, particularly translation, which are maintained by strong selection, the average selection coefficient for most nonparasitic genes is low albeit positive, compatible with observed positive correlation between genome size and effective population size. Free-living microbes evolve under stronger selection for gene retention than parasites. Different classes of MGE show a broad range of fitness effects, from the nearly neutral transposons to prophages, which are actively eliminated by selection. Genes involved in antiparasite defense, on average, incur a fitness cost to the host that is at least as high as the cost of plasmids. This cost is probably due to the adverse effects of autoimmunity and curtailment of horizontal gene transfer caused by the defense systems and selfish behavior of some of these systems, such as toxin–antitoxin and restriction modification modules. Transposons follow a biphasic dynamics, with bursts of gene proliferation followed by decay in the copy number that is quantitatively captured by the model. The horizontal gene transfer to loss ratio, but not duplication to loss ratio, correlates with genome size, potentially explaining increased abundance of neutral and costly elements in larger genomes.

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An Important Role for Purifying Selection in Archaeal Genome Evolution

mSystems ◽

10.1128/msystems.00112-17 ◽

2017 ◽

Vol 2 (5) ◽

Cited By ~ 1

Author(s):

Zhe Lyu ◽

Zhi-Gang Li ◽

Fei He ◽

Ziding Zhang

Keyword(s):

Genome Evolution ◽

Genome Size ◽

Genetic Drift ◽

Purifying Selection ◽

Fundamental Question ◽

Bacterial Genomes ◽

Noncoding Sequences ◽

Genome Complexity ◽

Prokaryotic Genomes ◽

Eukaryotic Feature

ABSTRACT The evolution of genome complexities is a fundamental question in biology. A hallmark of eukaryotic genome complexity is that larger genomes tend to have more noncoding sequences, which are believed to be minimal in archaeal and bacterial genomes. However, we found that archaeal genomes also possessed this eukaryotic feature while bacterial genomes did not. This could be predicted from our analysis of genetic drift, which showed relaxed purifying selection in larger archaeal genomes, also a eukaryotic feature. In contrast, the opposite was evident in bacterial genomes. As the null hypothesis of genome evolution, population genetic theory suggests that selection strength controls genome size. Through the process of genetic drift, this theory predicts that compact genomes are maintained by strong purifying selection while complex genomes are enabled by weak purifying selection. It offers a unifying framework that explains why prokaryotic genomes are much smaller than their eukaryotic counterparts. However, recent findings suggest that bigger prokaryotic genomes appear to experience stronger purifying selection, indicating that purifying selection may not dominate prokaryotic genome evolution. Since archaeal genomes were underrepresented in those studies, generalization of the conclusions to both archaeal and bacterial genomes may not be warranted. In this study, we revisited this matter by focusing on archaeal and bacterial genomes separately. We found that bigger bacterial genomes indeed experienced stronger purifying selection, but the opposite was observed in archaeal genomes. This new finding would predict an enrichment of noncoding sequences in large archaeal genomes, which was confirmed by an analysis of coding density. In contrast, coding density remained stable regardless of bacterial genome size. In conclusion, this study suggests that purifying selection may play a more important role in archaeal genome evolution than previously hypothesized, indicating that there could be a major difference between the evolutionary regimes of Archaea and Bacteria. IMPORTANCE The evolution of genome complexity is a fundamental question in biology. A hallmark of eukaryotic genome complexity is that larger genomes tend to have more noncoding sequences, which are believed to be minimal in archaeal and bacterial genomes. However, we found that archaeal genomes also possessed this eukaryotic feature while bacterial genomes did not. This could be predicted from our analysis on genetic drift, which showed a relaxation of purifying selection in larger archaeal genomes, also a eukaryotic feature. In contrast, the opposite was evident in bacterial genomes.

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panRGP: a pangenome-based method to predict genomic islands and explore their diversity

Bioinformatics ◽

10.1093/bioinformatics/btaa792 ◽

2020 ◽

Vol 36 (Supplement_2) ◽

pp. i651-i658 ◽

Cited By ~ 1

Author(s):

Adelme Bazin ◽

Guillaume Gautreau ◽

Claudine Médigue ◽

David Vallenet ◽

Alexandra Calteau

Keyword(s):

Escherichia Coli ◽

Gene Transfer ◽

Horizontal Gene Transfer ◽

Species Level ◽

Genomic Islands ◽

Genome Plasticity ◽

Reference Dataset ◽

Prokaryotic Genomes ◽

Ideal Approach ◽

Genomic Regions

Abstract Motivation Horizontal gene transfer (HGT) is a major source of variability in prokaryotic genomes. Regions of genome plasticity (RGPs) are clusters of genes located in highly variable genomic regions. Most of them arise from HGT and correspond to genomic islands (GIs). The study of those regions at the species level has become increasingly difficult with the data deluge of genomes. To date, no methods are available to identify GIs using hundreds of genomes to explore their diversity. Results We present here the panRGP method that predicts RGPs using pangenome graphs made of all available genomes for a given species. It allows the study of thousands of genomes in order to access the diversity of RGPs and to predict spots of insertions. It gave the best predictions when benchmarked along other GI detection tools against a reference dataset. In addition, we illustrated its use on metagenome assembled genomes by redefining the borders of the leuX tRNA hotspot, a well-studied spot of insertion in Escherichia coli. panRPG is a scalable and reliable tool to predict GIs and spots making it an ideal approach for large comparative studies. Availability and implementation The methods presented in the current work are available through the following software: https://github.com/labgem/PPanGGOLiN. Detailed results and scripts to compute the benchmark metrics are available at https://github.com/axbazin/panrgp_supdata.

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Complete Sequences of Two Plasmids Found in a Brazilian Bacillus thuringiensis Serovar israelensis Strain

Microbiology Resource Announcements ◽

10.1128/mra.00051-19 ◽

2019 ◽

Vol 8 (9) ◽

Author(s):

Fabrício S. Campos ◽

Fernando B. Cerqueira ◽

Gil R. Santos ◽

Eliseu J. G. Pereira ◽

Roberto F. T. Corrêia ◽

...

Keyword(s):

Bacillus Thuringiensis ◽

Gene Transfer ◽

Horizontal Gene Transfer ◽

Crucial Role ◽

Bacterial Genomes ◽

Content Type ◽

Complete Sequences

Plasmids play a crucial role in the evolution of bacterial genomes by mediating horizontal gene transfer. In this work, we sequenced two plasmids found in a Brazilian Bacillus thuringiensis serovar israelensis strain which showed 100% nucleotide identities with Bacillus thuringiensis serovar kurstaki plasmids.

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Comparative mitogenomics indicates respiratory competence in parasitic Viscum despite loss of complex I and extreme sequence divergence, and reveals horizontal gene transfer and remarkable variation in genome size

BMC Plant Biology ◽

10.1186/s12870-017-0992-8 ◽

2017 ◽

Vol 17 (1) ◽

Cited By ~ 26

Author(s):

Elizabeth Skippington ◽

Todd J. Barkman ◽

Danny W. Rice ◽

Jeffrey D. Palmer

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Genome Size ◽

Complex I ◽

Sequence Divergence

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Involvement of plastid, mitochondrial and nuclear genomes in plant-to-plant horizontal gene transfer

Acta Societatis Botanicorum Poloniae ◽

10.5586/asbp.2014.041 ◽

2014 ◽

Vol 83 (4) ◽

pp. 317-323 ◽

Cited By ~ 18

Author(s):

Maria Virginia Sanchez-Puerta

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Plant Mitochondria ◽

Genetic Material ◽

Single Copy ◽

Convincing Evidence ◽

Cell Contact ◽

Plant Mtdna ◽

Nuclear Genomes ◽

Foreign Genes

This review focuses on plant-to-plant horizontal gene transfer (HGT) involving the three DNA-containing cellular compartments. It highlights the great incidence of HGT in the mitochondrial genome (mtDNA) of angiosperms, the increasing number of examples in plant nuclear genomes, and the lack of any convincing evidence for HGT in the well-studied plastid genome of land plants. Most of the foreign mitochondrial genes are non-functional, generally found as pseudogenes in the recipient plant mtDNA that maintains its functional native genes. The few exceptions involve chimeric HGT, in which foreign and native copies recombine leading to a functional and single copy of the gene. Maintenance of foreign genes in plant mitochondria is probably the result of genetic drift, but a possible evolutionary advantage may be conferred through the generation of genetic diversity by gene conversion between native and foreign copies. Conversely, a few cases of nuclear HGT in plants involve functional transfers of novel genes that resulted in adaptive evolution. Direct cell-to-cell contact between plants (e.g. host-parasite relationships or natural grafting) facilitate the exchange of genetic material, in which HGT has been reported for both nuclear and mitochondrial genomes, and in the form of genomic DNA, instead of RNA. A thorough review of the literature indicates that HGT in mitochondrial and nuclear genomes of angiosperms is much more frequent than previously expected and that the evolutionary impact and mechanisms underlying plant-to-plant HGT remain to be uncovered.

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Effect of the environment on horizontal gene transfer between bacteria and archaea

PeerJ ◽

10.7717/peerj.3865 ◽

2017 ◽

Vol 5 ◽

pp. e3865 ◽

Cited By ~ 23

Author(s):

Clara A. Fuchsman ◽

Roy Eric Collins ◽

Gabrielle Rocap ◽

William J. Brazelton

Keyword(s):

High Temperature ◽

Gene Transfer ◽

Horizontal Gene Transfer ◽

Genome Size ◽

Thermophilic Bacteria ◽

Genetic Material ◽

Strongly Correlated ◽

Temperature Conditions ◽

Large Numbers ◽

Reciprocal Blast

BackgroundHorizontal gene transfer, the transfer and incorporation of genetic material between different species of organisms, has an important but poorly quantified role in the adaptation of microbes to their environment. Previous work has shown that genome size and the number of horizontally transferred genes are strongly correlated. Here we consider how genome size confuses the quantification of horizontal gene transfer because the number of genes an organism accumulates over time depends on its evolutionary history and ecological context (e.g., the nutrient regime for which it is adapted).ResultsWe investigated horizontal gene transfer between archaea and bacteria by first counting reciprocal BLAST hits among 448 bacterial and 57 archaeal genomes to find shared genes. Then we used the DarkHorse algorithm, a probability-based, lineage-weighted method (Podell & Gaasterland, 2007), to identify potential horizontally transferred genes among these shared genes. By removing the effect of genome size in the bacteria, we have identified bacteria with unusually large numbers of shared genes with archaea for their genome size. Interestingly, archaea and bacteria that live in anaerobic and/or high temperature conditions are more likely to share unusually large numbers of genes. However, high salt was not found to significantly affect the numbers of shared genes. Numbers of shared (genome size-corrected, reciprocal BLAST hits) and transferred genes (identified by DarkHorse) were strongly correlated. Thus archaea and bacteria that live in anaerobic and/or high temperature conditions are more likely to share horizontally transferred genes. These horizontally transferred genes are over-represented by genes involved in energy conversion as well as the transport and metabolism of inorganic ions and amino acids.ConclusionsAnaerobic and thermophilic bacteria share unusually large numbers of genes with archaea. This is mainly due to horizontal gene transfer of genes from the archaea to the bacteria.In general, these transfers are from archaea that live in similar oxygen and temperature conditions as the bacteria that receive the genes. Potential hotspots of horizontal gene transfer between archaea and bacteria include hot springs, marine sediments, and oil wells. Cold spots for horizontal transfer included dilute, aerobic, mesophilic environments such as marine and freshwater surface waters.

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Archaeal integrases and mechanisms of gene capture

Biochemical Society Transactions ◽

10.1042/bst0320222 ◽

2004 ◽

Vol 32 (2) ◽

pp. 222-226 ◽

Cited By ~ 46

Author(s):

Q. She ◽

B. Shen ◽

L. Chen

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Genome Evolution ◽

Trna Genes ◽

Gene Fragment ◽

Integrase Gene ◽

Site Specific ◽

Conjugative Plasmids ◽

Site Specific Integration ◽

Target Sites

Archaeal integrases facilitate the formation of two distinctive types of integrated element within archaeal chromosomes: the SSV type and pNOB8 type. The former carries a smaller N-terminal and a larger C-terminal integrase gene fragment, and the latter an intact integrase gene. All integrated elements overlap tRNA genes that were target sites for integration. It has been demonstrated that SSV (Sulfolobus spindle virus) viruses, carrying an SSV-type integrase gene, and conjugative plasmids, carrying a pNOB8-type integrase, are integrative elements. Two mechanisms have been proposed for stably maintaining an integrated element within archaeal chromosomes. There is also evidence for changes having occurred in the captured integrated elements present in archaeal genomes. Thus we infer that site-specific integration constitutes an important mechanism for horizontal gene transfer and genome evolution.

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