ShadowCaster: compositional methods under the shadow of phylogenetic models for the detection of horizontal gene transfer events in prokaryotes

AbstractHorizontal gene transfer (HGT) plays an important role in the evolution of many organisms, especially in prokaryotes where commonly occurs. Microbial communities can improve survival due to the evolutionary innovations induced by HGT events. Thus, several computational approaches have arisen to identify such events in recipient genomes. However, this has been proven to be a complex task due to the generation of a great number of false positives and the prediction disagreement among the existing methods. Phylogenetic reconstruction methods turned out to be the most reliable but they are not extensible to all genes/species and are computationally demanding when dealing with large datasets. On the other hand, the so-called surrogate methods that use heuristic solutions either based on nucleotide composition patterns or phyletic distribution of BLAST hits can be applied easily to genomic scale, however, they fail in identifying common HGT events. Here, we present ShadowCaster, a hybrid approach that sequentially combines compositional features under the shadow of phylogenetic models independent of tree reconstruction to improve the detection of HTG events in prokaryotes. ShadowCaster predicted successfully close and distant HTG events in both artificial and bacterial genomes. It detected HGT related to heavy metal resistance in the genome of Rhodanobacter denitrificans with higher accuracy than the most popular state-of-the-art computational approaches. ShadowCaster’s predictions showed the highest agreement among those obtained with other assayed methods. ShadowCaster is released as an open-source software under the GPLv3 license. Source code is hosted at https://github.com/dani2s/ShadowCaster and documentation at https://shadowcaster.readthedocs.io/en/latest/.

Download Full-text

ShadowCaster: Compositional Methods under the Shadow of Phylogenetic Models to Detect Horizontal Gene Transfers in Prokaryotes

Genes ◽

10.3390/genes11070756 ◽

2020 ◽

Vol 11 (7) ◽

pp. 756

Author(s):

Daniela Sánchez-Soto ◽

Guillermin Agüero-Chapin ◽

Vinicio Armijos-Jaramillo ◽

Yunierkis Perez-Castillo ◽

Eduardo Tejera ◽

...

Keyword(s):

Hybrid Approach ◽

Phylogenetic Reconstruction ◽

Heavy Metal Resistance ◽

Nucleotide Composition ◽

Metal Resistance ◽

Support Vector ◽

Computational Approaches ◽

Reconstruction Methods ◽

Genomic Scale ◽

Phylogenetic Models

Horizontal gene transfer (HGT) plays an important role for evolutionary innovations within prokaryotic communities and is a crucial event for their survival. Several computational approaches have arisen to identify HGT events in recipient genomes. However, this has been proven to be a complex task due to the generation of a great number of false positives and the prediction disagreement among the existing methods. Phylogenetic reconstruction methods turned out to be the most reliable ones, but they are not extensible to all genes/species and are computationally demanding when dealing with large datasets. In contrast, the so-called surrogate methods that use heuristic solutions either based on nucleotide composition patterns or phyletic distribution of BLAST hits can be applied easily to the genomic scale, but they fail in identifying common HGT events. Here, we present ShadowCaster, a hybrid approach that sequentially combines nucleotide composition-based predictions by support vector machines (SVMs) under the shadow of phylogenetic models independent of tree reconstruction, to improve the detection of HGT events in prokaryotes. ShadowCaster successfully predicted close and distant HGT events in both artificial and bacterial genomes. ShadowCaster detected HGT related to heavy metal resistance in the genome of Rhodanobacter denitrificans with higher accuracy than the most popular state-of-the-art computational approaches, encompassing most of the predicted cases made by other methods. ShadowCaster is released at the GitHub platform as an open-source software under the GPLv3 license.

Download Full-text

Horizontal Gene Transfer of PIB-Type ATPases among Bacteria Isolated from Radionuclide- and Metal-Contaminated Subsurface Soils

Applied and Environmental Microbiology ◽

10.1128/aem.72.5.3111-3118.2006 ◽

2006 ◽

Vol 72 (5) ◽

pp. 3111-3118 ◽

Cited By ~ 72

Author(s):

Robert J. Martinez ◽

Yanling Wang ◽

Melanie A. Raimondo ◽

Jonna M. Coombs ◽

Tamar Barkay ◽

...

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Field Research ◽

Pcr Primers ◽

Extreme Environment ◽

Heavy Metal Resistance ◽

Metal Resistance ◽

Oak Ridge ◽

Dna Base ◽

Toxic Concentrations

ABSTRACT Aerobic heterotrophs were isolated from subsurface soil samples obtained from the U.S. Department of Energy's (DOE) Field Research Center (FRC) located at Oak Ridge, Tenn. The FRC represents a unique, extreme environment consisting of highly acidic soils with cooccurring heavy metals, radionuclides, and high nitrate concentrations. Four hundred isolates obtained from contaminated soil were assayed for heavy metal resistance, and a smaller subset was assayed for tolerance to uranium. The vast majority of the isolates were gram-positive bacteria and belonged to the high-G+C- and low-G+C-content genera Arthrobacter and Bacillus, respectively. Genomic DNA from a randomly chosen subset of 50 Pb-resistant (Pbr) isolates was amplified with PCR primers specific for PIB-type ATPases (i.e., pbrA/cadA/zntA). A total of 10 pbrA/cadA/zntA loci exhibited evidence of acquisition by horizontal gene transfer. A remarkable dissemination of the horizontally acquired PIB-type ATPases was supported by unusual DNA base compositions and phylogenetic incongruence. Numerous Pbr PIB-type ATPase-positive FRC isolates belonging to the genus Arthrobacter tolerated toxic concentrations of soluble U(VI) (UO2 2+) at pH 4. These unrelated, yet synergistic, physiological traits observed in Arthrobacter isolates residing in the contaminated FRC subsurface may contribute to the survival of the organisms in such an extreme environment. This study is, to the best of our knowledge, the first study to report broad horizontal transfer of PIB-type ATPases in contaminated subsurface soils and is among the first studies to report uranium tolerance of aerobic heterotrophs obtained from the acidic subsurface at the DOE FRC.

Download Full-text

Comparative Genomic Analysis Uncovered Evolution of Pathogenicity Factors, Horizontal Gene Transfer Events, and Heavy Metal Resistance Traits in Citrus Canker Bacterium Xanthomonas citri subsp. citri

Frontiers in Microbiology ◽

10.3389/fmicb.2021.731711 ◽

2021 ◽

Vol 12 ◽

Author(s):

Chien-Jui Huang ◽

Ting-Li Wu ◽

Po-Xing Zheng ◽

Jheng-Yang Ou ◽

Hui-Fang Ni ◽

...

Keyword(s):

Heavy Metal ◽

Gene Transfer ◽

Horizontal Gene Transfer ◽

Resistance Genes ◽

Resistant Strain ◽

Management Practices ◽

Citrus Canker ◽

Heavy Metal Resistance ◽

Metal Resistance ◽

Pathogenicity Factors

Background: Worldwide citrus production is severely threatened by Asiatic citrus canker which is caused by the proteobacterium Xanthomonas citri subsp. citri. Foliar sprays of copper-based bactericides are frequently used to control plant bacterial diseases. Despite the sequencing of many X. citri strains, the genome diversity and distribution of genes responsible for metal resistance in X. citri subsp. citri strains from orchards with different management practices in Taiwan are not well understood.Results: The genomes of three X. citri subsp. citri strains including one copper-resistant strain collected from farms with different management regimes in Taiwan were sequenced by Illumina and Nanopore sequencing and assembled into complete circular chromosomes and plasmids. CRISPR spoligotyping and phylogenomic analysis indicated that the three strains were located in the same phylogenetic lineages and shared ∼3,000 core-genes with published X. citri subsp. citri strains. These strains differed mainly in the CRISPR repeats and pathogenicity-related plasmid-borne transcription activator-like effector (TALE)-encoding pthA genes. The copper-resistant strain has a unique, large copper resistance plasmid due to an unusual ∼40 kbp inverted repeat. Each repeat contains a complete set of the gene cluster responsible for copper and heavy metal resistance. Conversely, the copper sensitive strains carry no metal resistance genes in the plasmid. Through comparative analysis, the origin and evolution of the metal resistance clusters was resolved.Conclusion: Chromosomes remained constant among three strains collected in Taiwan, but plasmids likely played an important role in maintaining pathogenicity and developing bacterial fitness in the field. The evolution of pathogenicity factors and horizontal gene transfer events were observed in the three strains. These data suggest that agricultural management practices could be a potential trigger for the evolution of citrus canker pathogens. The decrease in the number of CRISPR repeats and pthA genes might be the result of adaptation to a less stressful environment. The metal resistance genes in the copper resistant X. citri strain likely originated from the Mauritian strain not the local copper-resistant X. euvesicatoria strain. This study highlights the importance of plasmids as ‘vehicles’ for exchanging genetic elements between plant pathogenic bacteria and contributing to bacterial adaptation to the environment.

Download Full-text

Faculty Opinions recommendation of Ancient horizontal gene transfer can benefit phylogenetic reconstruction.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1046784.496796 ◽

2006 ◽

Author(s):

Nicolas Galtier

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Phylogenetic Reconstruction

Download Full-text

Horizontal gene transfer in human-associated microorganisms inferred by phylogenetic reconstruction and reconciliation

Scientific Reports ◽

10.1038/s41598-019-42227-5 ◽

2019 ◽

Vol 9 (1) ◽

Cited By ~ 15

Author(s):

Hyeonsoo Jeong ◽

Bushra Arif ◽

Gustavo Caetano-Anollés ◽

Kyung Mo Kim ◽

Arshan Nasir

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Phylogenetic Reconstruction

Download Full-text

Horizontal gene transfer from extinct and extant lineages: biological innovation and the coral of life

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2009.0033 ◽

2009 ◽

Vol 364 (1527) ◽

pp. 2229-2239 ◽

Cited By ~ 49

Author(s):

Gregory P. Fournier ◽

Jinling Huang ◽

J. Peter Gogarten

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Evolutionary History ◽

Phylogenetic Reconstruction ◽

Gene Trees ◽

Individual Gene ◽

Evolution Of Life ◽

Domains Of Life ◽

Life On Earth ◽

Simple Tree

Horizontal gene transfer (HGT) is often considered to be a source of error in phylogenetic reconstruction, causing individual gene trees within an organismal lineage to be incongruent, obfuscating the ‘true’ evolutionary history. However, when identified as such, HGTs between divergent organismal lineages are useful, phylogenetically informative characters that can provide insight into evolutionary history. Here, we discuss several distinct HGT events involving all three domains of life, illustrating the selective advantages that can be conveyed via HGT, and the utility of HGT in aiding phylogenetic reconstruction and in dating the relative sequence of speciation events. We also discuss the role of HGT from extinct lineages, and its impact on our understanding of the evolution of life on Earth. Organismal phylogeny needs to incorporate reticulations; a simple tree does not provide an accurate depiction of the processes that have shaped life's history.

Download Full-text

Horizontal Gene Transfer of Antibiotic Resistance from Acinetobacter baylyi to Escherichia coli on Lettuce and Subsequent Antibiotic Resistance Transmission to the Gut Microbiome

mSphere ◽

10.1128/msphere.00329-20 ◽

2020 ◽

Vol 5 (3) ◽

Cited By ~ 2

Author(s):

Marlène Maeusli ◽

Bosul Lee ◽

Sarah Miller ◽

Zeferino Reyna ◽

Peggy Lu ◽

...

Keyword(s):

Antibiotic Resistance ◽

Gene Transfer ◽

Horizontal Gene Transfer ◽

Resistance Genes ◽

Gut Microbiome ◽

Acinetobacter Baylyi ◽

Antibiotic Resistant ◽

Content Type ◽

Plant Foods ◽

Link Type

ABSTRACT Agricultural use of antibiotics is recognized by the U.S. Centers for Disease Control and Prevention as a major contributor to antibiotic-resistant infections. While most One Health attention has been on the potential for antibiotic resistance transmission from livestock and contaminated meat products to people, plant foods are fundamental to the food chain for meat eaters and vegetarians alike. We hypothesized that environmental bacteria that colonize plant foods may serve as platforms for the persistence of antibiotic-resistant bacteria and for horizontal gene transfer of antibiotic-resistant genes. Donor Acinetobacter baylyi and recipient Escherichia coli were cocultured in vitro, in planta on lettuce, and in vivo in BALB/c mice. We showed that nonpathogenic, environmental A. baylyi is capable of transferring plasmids conferring antibiotic resistance to E. coli clinical isolates on lettuce leaf discs. Furthermore, transformant E. coli from the in planta assay could then colonize the mouse gut microbiome. The target antibiotic resistance plasmid was identified in mouse feces up to 5 days postinfection. We specifically identified in vivo transfer of the plasmid to resident Klebsiella pneumoniae in the mouse gut. Our findings highlight the potential for environmental bacteria exposed to antibiotics to transmit resistance genes to mammalian pathogens during ingestion of leafy greens. IMPORTANCE Previous efforts have correlated antibiotic-fed livestock and meat products with respective antibiotic resistance genes, but virtually no research has been conducted on the transmission of antibiotic resistance from plant foods to the mammalian gut (C. S. Hölzel, J. L. Tetens, and K. Schwaiger, Pathog Dis 15:671–688, 2018, https://doi.org/10.1089/fpd.2018.2501; C. M. Liu et al., mBio 9:e00470-19, 2018, https://doi.org/10.1128/mBio.00470-18; B. Spellberg et al., NAM Perspectives, 2016, https://doi.org/10.31478/201606d; J. O’Neill, Antimicrobials in agriculture and the environment, 2015; Centers for Disease Control and Prevention, Antibiotic resistance threats in the United States, 2019). Here, we sought to determine if horizontal transmission of antibiotic resistance genes can occur between lettuce and the mammalian gut microbiome, using a mouse model. Furthermore, we have created a new model to study horizontal gene transfer on lettuce leaves using an antibiotic-resistant transformant of A. baylyi (AbzeoR).

Download Full-text

Genetic relatedness of Streptococcus dysgalactiae isolates causing recurrent bacteraemia

Journal of Medical Microbiology ◽

10.1099/jmm.0.001330 ◽

2021 ◽

Author(s):

Erik Senneby ◽

Björn Hallström ◽

Magnus Rasmussen

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Phylogenetic Trees ◽

Genetic Relatedness ◽

Sequence Similarity ◽

Streptococcus Dysgalactiae ◽

High Sequence Similarity ◽

Content Type ◽

Link Type ◽

Clonal Origin

Introduction. Streptococcus dysgalactiae subspecies equisimilis (SDSE) is becoming increasingly recognized as an important human pathogen. Recurrent bacteremia with SDSE has been described previously. Aim. The aims of the study were to establish the genetic relatedness of SDSE isolates with emm-type stG643 that had caused recurrent bacteraemia in three patients and to search for signs of horizontal gene transfer of the emm gene in a collection of SDSE stG643 genomes. Hypothesis. Recurring SDSE bacteremia is caused by the same clone in one patient. Methodology. Whole genome sequencing of 22 clinical SDSE stG643 isolates was performed, including three paired blood culture isolates and sixteen isolates from various sites. All assemblies were aligned to a reference assembly and SNPs were extracted. A total of 53 SDSE genomes were downloaded from GenBank. Two phylogenetic trees, including all 75 SDSE isolates, were created. One tree was based on the emm gene only and one tree was based on all variable positions in the genomes. Results. The genomes from the three pairs of SDSE isolates showed high sequence similarity (1–17 SNPs difference between the pairs), whereas the median SNP difference between the 22 isolates in our collection was 1694 (range 1–11257). The paired isolates were retrieved with 7–53 months between episodes. The 22 SDSE isolates from our collection formed a cluster in the phylogenetic tree based on the emm gene, while they were more scattered in the tree based on all variable positions. Conclusions. Our results show that the paired isolates were of the same clonal origin, which in turn supports carriage between bacteraemia episodes. The phylogenetic analysis indicates that horizontal gene transfer of the emm-gene between some of the SDSE isolates has occurred.

Download Full-text