Visual Evidence of Horizontal Gene Transfer between Plants and Bacteria in the Phytosphere of Transplastomic Tobacco

ABSTRACT Plant surfaces, colonized by numerous and diverse bacterial species, are often considered hot spots for horizontal gene transfer (HGT) between plants and bacteria. Plant DNA released during the degradation of plant tissues can persist and remain biologically active for significant periods of time, suggesting that soil or plant-associated bacteria could be in direct contact with plant DNA. In addition, nutrients released during the decaying process may provide a copiotrophic environment conducive for opportunistic microbial growth. Using Acinetobacter baylyi strain BD413 and transplastomic tobacco plants harboring the aadA gene as models, the objective of this study was to determine whether specific niches could be shown to foster bacterial growth on intact or decaying plant tissues, to develop a competence state, and to possibly acquire exogenous plant DNA by natural transformation. Visualization of HGT in situ was performed using A. baylyi strain BD413(rbcL-ΔPaadA::gfp) carrying a promoterless aadA::gfp fusion. Both antibiotic resistance and green fluorescence phenotypes were restored in recombinant bacterial cells after homologous recombination with transgenic plant DNA. Opportunistic growth occurred on decaying plant tissues, and a significant proportion of the bacteria developed a competence state. Quantification of transformants clearly supported the idea that the phytosphere constitutes a hot spot for HGT between plants and bacteria. The nondisruptive approach used to visualize transformants in situ provides new insights into environmental factors influencing HGT for plant tissues.

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An Evolutionary Link between Natural Transformation and CRISPR Adaptive Immunity

mBio ◽

10.1128/mbio.00309-12 ◽

2012 ◽

Vol 3 (5) ◽

Cited By ~ 52

Author(s):

Peter Jorth ◽

Marvin Whiteley

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Bacterial Diversity ◽

Natural Transformation ◽

Bacterial Species ◽

Comparative Genomic ◽

Content Type ◽

Immune Systems ◽

Adaptive Immune ◽

Adaptive Immune Systems

ABSTRACTNatural transformation by competent bacteria is a primary means of horizontal gene transfer; however, evidence that competence drives bacterial diversity and evolution has remained elusive. To test this theory, we used a retrospective comparative genomic approach to analyze the evolutionary history ofAggregatibacter actinomycetemcomitans, a bacterial species with both competent and noncompetent sister strains. Through comparative genomic analyses, we reveal that competence is evolutionarily linked to genomic diversity and speciation. Competence loss occurs frequently during evolution and is followed by the loss of clustered regularly interspaced short palindromic repeats (CRISPRs), bacterial adaptive immune systems that protect against parasitic DNA. Relative to noncompetent strains, competent bacteria have larger genomes containing multiple rearrangements. In contrast, noncompetent bacterial genomes are extremely stable but paradoxically susceptible to infective DNA elements, which contribute to noncompetent strain genetic diversity. Moreover, incomplete noncompetent strain CRISPR immune systems are enriched for self-targeting elements, which suggests that the CRISPRs have been co-opted for bacterial gene regulation, similar to eukaryotic microRNAs derived from the antiviral RNA interference pathway.IMPORTANCEThe human microbiome is rich with thousands of diverse bacterial species. One mechanism driving this diversity is horizontal gene transfer by natural transformation, whereby naturally competent bacteria take up environmental DNA and incorporate new genes into their genomes. Competence is theorized to accelerate evolution; however, attempts to test this theory have proved difficult. Through genetic analyses of the human periodontal pathogenAggregatibacter actinomycetemcomitans, we have discovered an evolutionary connection between competence systems promoting gene acquisition and CRISPRs (clustered regularly interspaced short palindromic repeats), adaptive immune systems that protect bacteria against genetic parasites. We show that competentA. actinomycetemcomitansstrains have numerous redundant CRISPR immune systems, while noncompetent bacteria have lost their CRISPR immune systems because of inactivating mutations. Together, the evolutionary data linking the evolution of competence and CRISPRs reveals unique mechanisms promoting genetic heterogeneity and the rise of new bacterial species, providing insight into complex mechanisms underlying bacterial diversity in the human body.

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Acquisition of Beta-Lactamase by Neisseria meningitidis through Possible Horizontal Gene Transfer

Antimicrobial Agents and Chemotherapy ◽

10.1128/aac.00831-18 ◽

2018 ◽

Vol 62 (9) ◽

Cited By ~ 7

Author(s):

Eva Hong ◽

Ala-Eddine Deghmane ◽

Muhamed-Kheir Taha

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Genome Sequencing ◽

Meningococcal Disease ◽

Bacterial Species ◽

Whole Genome ◽

Beta Lactamase ◽

Content Type ◽

Beta Lactamases ◽

Lactamase Gene

ABSTRACT We report the detection in France of a beta-lactamase-producing invasive meningococcal isolate. Whole-genome sequencing of the isolate revealed a ROB-1-type beta-lactamase gene that is frequently encountered in Haemophilus influenzae, suggesting horizontal transfer between isolates of these bacterial species. Beta-lactamases are exceptional in meningococci, with no reports for more than 2 decades. This report is worrying, as the expansion of such isolates may jeopardize the effective treatment against invasive meningococcal disease.

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Phylogenomic Analyses of Non-Dikarya Fungi Supports Horizontal Gene Transfer Driving Diversification of Secondary Metabolism in the Amphibian Gastrointestinal Symbiont, Basidiobolus

G3 Genes|Genome|Genetics ◽

10.1534/g3.120.401516 ◽

2020 ◽

Vol 10 (9) ◽

pp. 3417-3433

Author(s):

Javier F Tabima ◽

Ian A Trautman ◽

Ying Chang ◽

Yan Wang ◽

Stephen Mondo ◽

...

Keyword(s):

Gene Expression ◽

Gene Transfer ◽

Horizontal Gene Transfer ◽

Secondary Metabolism ◽

Gene Clusters ◽

Biologically Active ◽

Constitutive Gene Expression ◽

Gut Symbionts ◽

Phylogenomic Analyses ◽

Siderophore Activity

Abstract Research into secondary metabolism (SM) production by fungi has resulted in the discovery of diverse, biologically active compounds with significant medicinal applications. The fungi rich in SM production are taxonomically concentrated in the subkingdom Dikarya, which comprises the phyla Ascomycota and Basidiomycota. Here, we explore the potential for SM production in Mucoromycota and Zoopagomycota, two phyla of nonflagellated fungi that are not members of Dikarya, by predicting and identifying core genes and gene clusters involved in SM. The majority of non-Dikarya have few genes and gene clusters involved in SM production except for the amphibian gut symbionts in the genus Basidiobolus. Basidiobolus genomes exhibit an enrichment of SM genes involved in siderophore, surfactin-like, and terpene cyclase production, all these with evidence of constitutive gene expression. Gene expression and chemical assays also confirm that Basidiobolus has significant siderophore activity. The expansion of SMs in Basidiobolus are partially due to horizontal gene transfer from bacteria, likely as a consequence of its ecology as an amphibian gut endosymbiont.

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Lines of Evidence for Horizontal Gene Transfer of a Phenazine Producing Operon into Multiple Bacterial Species

Journal of Molecular Evolution ◽

10.1007/s00239-009-9198-5 ◽

2009 ◽

Vol 68 (2) ◽

pp. 171-185 ◽

Cited By ~ 27

Author(s):

David A. Fitzpatrick

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Bacterial Species ◽

Lines Of Evidence

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Inter-species population dynamics enhance microbial horizontal gene transfer and spread of antibiotic resistance

eLife ◽

10.7554/elife.25950 ◽

2017 ◽

Vol 6 ◽

Cited By ~ 48

Author(s):

Robert M Cooper ◽

Lev Tsimring ◽

Jeff Hasty

Keyword(s):

Antibiotic Resistance ◽

Gene Transfer ◽

Horizontal Gene Transfer ◽

Disease Control ◽

Multi Drug Resistance ◽

Acinetobacter Baylyi ◽

Adaptive Resistance ◽

Population Dynamic Model ◽

Control And Prevention ◽

Centers For Disease Control

Horizontal gene transfer (HGT) plays a major role in the spread of antibiotic resistance. Of particular concern are Acinetobacter baumannii bacteria, which recently emerged as global pathogens, with nosocomial mortality rates reaching 19–54% (Centers for Disease Control and Prevention, 2013; Joly Guillou, 2005; Talbot et al., 2006). Acinetobacter gains antibiotic resistance remarkably rapidly (Antunes et al., 2014; Joly Guillou, 2005), with multi drug-resistance (MDR) rates exceeding 60% (Antunes et al., 2014; Centers for Disease Control and Prevention, 2013). Despite growing concern (Centers for Disease Control and Prevention, 2013; Talbot et al., 2006), the mechanisms underlying this extensive HGT remain poorly understood (Adams et al., 2008; Fournier et al., 2006; Imperi et al., 2011; Ramirez et al., 2010; Wilharm et al., 2013). Here, we show bacterial predation by Acinetobacter baylyi increases cross-species HGT by orders of magnitude, and we observe predator cells functionally acquiring adaptive resistance genes from adjacent prey. We then develop a population-dynamic model quantifying killing and HGT on solid surfaces. We show DNA released via cell lysis is readily available for HGT and may be partially protected from the environment, describe the effects of cell density, and evaluate potential environmental inhibitors. These findings establish a framework for understanding, quantifying, and combating HGT within the microbiome and the emergence of MDR super-bugs.

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Metabolism of Toxic Sugars by Strains of the Bee Gut Symbiont Gilliamella apicola

mBio ◽

10.1128/mbio.01326-16 ◽

2016 ◽

Vol 7 (6) ◽

Cited By ~ 72

Author(s):

Hao Zheng ◽

Alex Nishida ◽

Waldan K. Kwong ◽

Hauke Koch ◽

Philipp Engel ◽

...

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Honey Bees ◽

Bacterial Species ◽

Bumble Bees ◽

Rrna Gene ◽

Phosphotransferase System ◽

Metabolic Potential ◽

Social Bees ◽

Gene Similarity

ABSTRACT Social bees collect carbohydrate-rich food to support their colonies, and yet, certain carbohydrates present in their diet or produced through the breakdown of pollen are toxic to bees. The gut microbiota of social bees is dominated by a few core bacterial species, including the Gram-negative species Gilliamella apicola . We isolated 42 strains of G. apicola from guts of honey bees and bumble bees and sequenced their genomes. All of the G. apicola strains share high 16S rRNA gene similarity, but they vary extensively in gene repertoires related to carbohydrate metabolism. Predicted abilities to utilize different sugars were verified experimentally. Some strains can utilize mannose, arabinose, xylose, or rhamnose (monosaccharides that can cause toxicity in bees) as their sole carbon and energy source. All of the G. apicola strains possess a manO -associated mannose family phosphotransferase system; phylogenetic analyses suggest that this was acquired from Firmicutes through horizontal gene transfer. The metabolism of mannose is specifically dependent on the presence of mannose-6-phosphate isomerase (MPI). Neither growth rates nor the utilization of glucose and fructose are affected in the presence of mannose when the gene encoding MPI is absent from the genome, suggesting that mannose is not taken up by G. apicola strains which harbor the phosphotransferase system but do not encode the MPI. Given their ability to simultaneously utilize glucose, fructose, and mannose, as well as the ability of many strains to break down other potentially toxic carbohydrates, G. apicola bacteria may have key roles in improving dietary tolerances and maintaining the health of their bee hosts. IMPORTANCE Bees are important pollinators of agricultural plants. Our study documents the ability of Gilliamella apicola , a dominant gut bacterium in honey bees and bumble bees, to utilize several sugars that are harmful to bee hosts. Using genome sequencing and growth assays, we found that the ability to metabolize certain toxic carbohydrates is directly correlated with the presence of their respective degradation pathways, indicating that metabolic potential can be accurately predicted from genomic data in these gut symbionts. Strains vary considerably in their range of utilizable carbohydrates, which likely reflects historical horizontal gene transfer and gene deletion events. Unlike their bee hosts, G. apicola bacteria are not detrimentally affected by growth on mannose-containing medium, even in strains that cannot metabolize this sugar. These results suggest that G. apicola may be an important player in modulating nutrition in the bee gut, with ultimate effects on host health.

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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).

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Reconstructing the Phylogeny of Corynebacteriales while Accounting for Horizontal Gene Transfer

Genome Biology and Evolution ◽

10.1093/gbe/evaa058 ◽

2020 ◽

Vol 12 (4) ◽

pp. 381-395

Author(s):

Nilson Da Rocha Coimbra ◽

Aristoteles Goes-Neto ◽

Vasco Azevedo ◽

Aïda Ouangraoua

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Phylogenetic Trees ◽

Bacterial Species ◽

Gene Tree ◽

Gene Families ◽

Common Mechanism ◽

Species Trees ◽

Bacterial Phylogeny ◽

Homologous Genes

Abstract Horizontal gene transfer is a common mechanism in Bacteria that has contributed to the genomic content of existing organisms. Traditional methods for estimating bacterial phylogeny, however, assume only vertical inheritance in the evolution of homologous genes, which may result in errors in the estimated phylogenies. We present a new method for estimating bacterial phylogeny that accounts for the presence of genes acquired by horizontal gene transfer between genomes. The method identifies and corrects putative transferred genes in gene families, before applying a gene tree-based summary method to estimate bacterial species trees. The method was applied to estimate the phylogeny of the order Corynebacteriales, which is the largest clade in the phylum Actinobacteria. We report a collection of 14 phylogenetic trees on 360 Corynebacteriales genomes. All estimated trees display each genus as a monophyletic clade. The trees also display several relationships proposed by past studies, as well as new relevant relationships between and within the main genera of Corynebacteriales: Corynebacterium, Mycobacterium, Nocardia, Rhodococcus, and Gordonia. An implementation of the method in Python is available on GitHub at https://github.com/UdeS-CoBIUS/EXECT (last accessed April 2, 2020).

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Involvement of β-Carbonic Anhydrase Genes in Bacterial Genomic Islands and Their Horizontal Transfer to Protists

Applied and Environmental Microbiology ◽

10.1128/aem.00771-18 ◽

2018 ◽

Vol 84 (15) ◽

Cited By ~ 3

Author(s):

Reza Zolfaghari Emameh ◽

Harlan R. Barker ◽

Vesa P. Hytönen ◽

Seppo Parkkila

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Carbonic Anhydrase ◽

Horizontal Transfer ◽

Bacterial Species ◽

Critical Role ◽

Genomic Islands ◽

Ph Homeostasis ◽

Gene Sequences ◽

Biochemical Pathways

ABSTRACT Genomic islands (GIs) are a type of mobile genetic element (MGE) that are present in bacterial chromosomes. They consist of a cluster of genes that produce proteins that contribute to a variety of functions, including, but not limited to, the regulation of cell metabolism, antimicrobial resistance, pathogenicity, virulence, and resistance to heavy metals. The genes carried in MGEs can be used as a trait reservoir in times of adversity. Transfer of genes using MGEs, occurring outside reproduction, is called horizontal gene transfer (HGT). Previous data have shown that numerous HGT events have occurred through endosymbiosis between prokaryotes and eukaryotes. β-Carbonic anhydrase (β-CA) enzymes play a critical role in the biochemical pathways of many prokaryotes and eukaryotes. We previously suggested the horizontal transfer of β-CA genes from plasmids of some prokaryotic endosymbionts to their protozoan hosts. In this study, we set out to identify β-CA genes that might have been transferred between prokaryotic and protist species through HGT in GIs. Therefore, we investigated prokaryotic chromosomes containing β-CA-encoding GIs and utilized multiple bioinformatics tools to reveal the distinct movements of β-CA genes among a wide variety of organisms. Our results identify the presence of β-CA genes in GIs of several medically and industrially relevant bacterial species, and phylogenetic analyses reveal multiple cases of likely horizontal transfer of β-CA genes from GIs of ancestral prokaryotes to protists. IMPORTANCE The evolutionary process is mediated by mobile genetic elements (MGEs), such as genomic islands (GIs). A gene or set of genes in the GIs is exchanged between and within various species through horizontal gene transfer (HGT). Based on the crucial role that GIs can play in bacterial survival and proliferation, they were introduced as environment- and pathogen-associated factors. Carbonic anhydrases (CAs) are involved in many critical biochemical pathways, such as the regulation of pH homeostasis and electrolyte transfer. Among the six evolutionary families of CAs, β-CA gene sequences are present in many bacterial species, which can be horizontally transferred to protists during evolution. This study shows the involvement of bacterial β-CA gene sequences in the GIs and suggests their horizontal transfer to protists during evolution.

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