Inter-domain Horizontal Gene Transfer of Nickel-binding Superoxide Dismutase

AbstractThe ability of aerobic microorganisms to regulate internal and external concentrations of the reactive oxygen species (ROS) superoxide directly influences the health and viability of cells. Superoxide dismutases (SODs) are the primary regulatory enzymes that are used by microorganisms to degrade superoxide. SOD is not one, but three separate, non-homologous enzymes that perform the same function. Thus, the evolutionary history of genes encoding for different SOD enzymes is one of convergent evolution, which reflects environmental selection brought about by an oxygenated atmosphere, changes in metal availability, and opportunistic horizontal gene transfer (HGT). In this study we examine the phylogenetic history of the protein sequence encoding for the nickel-binding metalloform of the SOD enzyme (SodN). A comparison of organismal and SodN protein phylogenetic trees reveals several instances of HGT, including multiple inter-domain transfers of the sodN gene from the bacterial domain to the archaeal domain. Nearly half of the archaeal members with sodN live in the photic zone of the marine water column. The sodN gene is widespread and characterized by apparent vertical gene transfer in some sediment-associated lineages within the Actinobacteriota (Actinobacteria) and Chloroflexota (Chloroflexi) phyla, suggesting the ancestral sodN likely originated in one of these clades before expanding its taxonomic and biogeographic distribution to additional microbial groups in the surface ocean in response to decreasing iron availability. In addition to decreasing iron quotas, nickel-binding SOD has the added benefit of withstanding high reactant and product ROS concentrations without damaging the enzyme, making it particularly well suited for the modern surface ocean.

Download Full-text

Novel 4-Chlorophenol Degradation Gene Cluster and Degradation Route via Hydroxyquinol in Arthrobacter chlorophenolicus A6

Applied and Environmental Microbiology ◽

10.1128/aem.71.11.6538-6544.2005 ◽

2005 ◽

Vol 71 (11) ◽

pp. 6538-6544 ◽

Cited By ~ 81

Author(s):

Karolina Nordin ◽

Maria Unell ◽

Janet K. Jansson

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Gene Cluster ◽

Microbial Degradation ◽

Codon Bias ◽

Sequence Similarity ◽

Open Reading Frames ◽

Genes Encoding ◽

Arthrobacter Chlorophenolicus ◽

Reading Frames

ABSTRACT Arthrobacter chlorophenolicus A6, a previously described 4-chlorophenol-degrading strain, was found to degrade 4-chlorophenol via hydroxyquinol, which is a novel route for aerobic microbial degradation of this compound. In addition, 10 open reading frames exhibiting sequence similarity to genes encoding enzymes involved in chlorophenol degradation were cloned and designated part of a chlorophenol degradation gene cluster (cph genes). Several of the open reading frames appeared to encode enzymes with similar functions; these open reading frames included two genes, cphA-I and cphA-II, which were shown to encode functional hydroxyquinol 1,2-dioxygenases. Disruption of the cphA-I gene yielded a mutant that exhibited negligible growth on 4-chlorophenol, thereby linking the cph gene cluster to functional catabolism of 4-chlorophenol in A. chlorophenolicus A6. The presence of a resolvase pseudogene in the cph gene cluster together with analyses of the G+C content and codon bias of flanking genes suggested that horizontal gene transfer was involved in assembly of the gene cluster during evolution of the ability of the strain to grow on 4-chlorophenol.

Download Full-text

Adaptation by Ancient Horizontal Acquisition of Butyrate Metabolism Genes in Aggregatibacter actinomycetemcomitans

mBio ◽

10.1128/mbio.03581-20 ◽

2021 ◽

Vol 12 (2) ◽

Author(s):

Ahmed M. Moustafa ◽

Senthil Kumar Velusamy ◽

Lidiya Denu ◽

Apurva Narechania ◽

Daniel H. Fine ◽

...

Keyword(s):

Phylogenetic Analysis ◽

Gene Transfer ◽

Horizontal Gene Transfer ◽

Strong Association ◽

Aggregatibacter Actinomycetemcomitans ◽

Short Chain ◽

Oral Microbiota ◽

Content Type ◽

History Of ◽

The Impact

ABSTRACT Like the bacterial residents of the human gut, it is likely that many of the species in the human oral microbiota have evolved to better occupy and persist in their niche. Aggregatibacter actinomycetemcomitans (Aa) is both a common colonizer of the oral cavity and has been implicated in the pathogenesis of periodontal disease. Here, we present a whole-genome phylogenetic analysis of Aa isolates from humans and nonhuman primates that revealed an ancient origin for this species and a long history of association with the Catarrhini, the lineage that includes Old World monkeys (OWM) and humans. Further genomic analysis showed a strong association with the presence of a short-chain fatty acid (SCFA) catabolism locus (atoRDAEB) in many human isolates that was absent in almost all nonhuman OWM isolates. We show that this locus was likely acquired through horizontal gene transfer. When grown under conditions that are similar to those at the subgingival site of periodontitis (anaerobic, SCFA replete), Aa strains with atoRDAEB formed robust biofilms and showed upregulation of genes involved in virulence, colonization, and immune evasion. Both an isogenic deletion mutant and nonhuman primate isolates lacking the ato locus failed to grow in a robust biofilm under these conditions, but grew well under the carbohydrate-rich conditions similar to those found above the gumline. We propose that the acquisition of the ato locus was a key evolutionary step allowing Aa to utilize SCFAs, adapt, and modulate subgingival disease. IMPORTANCE There has been considerable interest in the impact of short-chain fatty acids (SCFAs) on inflammatory effects related to the microbiome. Here, we present evidence that SCFAs may also be important in disease by providing an energy source or disease-associated cue for colonizing pathogens. We propose that SCFAs allow Aggregatibacter actinomycetemcomitans (Aa) to adapt to the subgingival anaerobic environment, which is the site of human periodontitis. Under anaerobic, SCFA-rich conditions, human-derived Aa strains that possess butyrate metabolism genes form strong biofilms and upregulate virulence genes. Our phylogenetic analysis highlights a long history of evolution of Aa with its primate hosts and suggests that the acquisition of butyrate metabolism genes may have been a critical step in allowing Aa to colonize a new niche and cause disease in humans. Overall, this study highlights the important role that horizontal gene transfer may play in microbial adaptation and the evolution of infectious disease.

Download Full-text

The Linguistics of Bacterial Conflict Systems Reveal Ancient Origins of Eukaryotic Innate Immunity

Journal of Bacteriology ◽

10.1128/jb.00507-20 ◽

2020 ◽

Vol 202 (24) ◽

Author(s):

Emily M. Kibby ◽

Aaron T. Whiteley

Keyword(s):

Innate Immunity ◽

Gene Transfer ◽

Horizontal Gene Transfer ◽

Evolutionary History ◽

Protein Domains ◽

Arms Race ◽

Bacterial Populations ◽

Defense Systems ◽

History Of ◽

Novel Protein

ABSTRACT The arms race between bacteria and their competitors has produced an astounding variety of conflict systems that are shared via horizontal gene transfer across bacterial populations. In this issue of the Journal of Bacteriology, Burroughs and Aravind investigate how these biological conflict systems have been mixed and matched into new configurations, often with novel protein domains (A. M. Burroughs and L. Aravind, J Bacteriol 202:e00365-20, 2020, https://doi.org/10.1128/JB.00365-20). The authors additionally characterize the evolutionary history of genes in eukaryotes that appear to have been acquired from these prokaryotic defense systems.

Download Full-text

Granick revisited: Synthesizing evolutionary and ecological evidence for the late origin of bacteriochlorophyll via ghost lineages and horizontal gene transfer

PLoS ONE ◽

10.1371/journal.pone.0239248 ◽

2021 ◽

Vol 16 (1) ◽

pp. e0239248 ◽

Cited By ~ 1

Author(s):

Lewis M. Ward ◽

Patrick M. Shih

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Evolutionary History ◽

Photosynthetic Bacteria ◽

Photosynthetic Apparatus ◽

Metagenomic Sequencing ◽

Crown Group ◽

Environmental Diversity ◽

Chlorophyll Pigments ◽

History Of

Photosynthesis—both oxygenic and more ancient anoxygenic forms—has fueled the bulk of primary productivity on Earth since it first evolved more than 3.4 billion years ago. However, the early evolutionary history of photosynthesis has been challenging to interpret due to the sparse, scattered distribution of metabolic pathways associated with photosynthesis, long timescales of evolution, and poor sampling of the true environmental diversity of photosynthetic bacteria. Here, we reconsider longstanding hypotheses for the evolutionary history of phototrophy by leveraging recent advances in metagenomic sequencing and phylogenetics to analyze relationships among phototrophic organisms and components of their photosynthesis pathways, including reaction centers and individual proteins and complexes involved in the multi-step synthesis of (bacterio)-chlorophyll pigments. We demonstrate that components of the photosynthetic apparatus have undergone extensive, independent histories of horizontal gene transfer. This suggests an evolutionary mode by which modular components of phototrophy are exchanged between diverse taxa in a piecemeal process that has led to biochemical innovation. We hypothesize that the evolution of extant anoxygenic photosynthetic bacteria has been spurred by ecological competition and restricted niches following the evolution of oxygenic Cyanobacteria and the accumulation of O2 in the atmosphere, leading to the relatively late evolution of bacteriochlorophyll pigments and the radiation of diverse crown group anoxygenic phototrophs. This hypothesis expands on the classic “Granick hypothesis” for the stepwise evolution of biochemical pathways, synthesizing recent expansion in our understanding of the diversity of phototrophic organisms as well as their evolving ecological context through Earth history.

Download Full-text

Granick Revisited: Synthesizing Evolutionary and Ecological Evidence for the Late Origin of Bacteriochlorophyll via Ghost Lineages and Horizontal Gene Transfer

10.1101/2020.09.01.277905 ◽

2020 ◽

Cited By ~ 2

Author(s):

Lewis M. Ward ◽

Patrick M. Shih

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Evolutionary History ◽

Photosynthetic Bacteria ◽

Photosynthetic Apparatus ◽

Metagenomic Sequencing ◽

Crown Group ◽

Environmental Diversity ◽

Chlorophyll Pigments ◽

History Of

AbstractPhotosynthesis—both oxygenic and more ancient anoxygenic forms—has fueled the bulk of primary productivity on Earth since it first evolved more than 3.4 billion years ago. However, the early evolutionary history of photosynthesis has been challenging to interpret due to the sparse, scattered distribution of metabolic pathways associated with photosynthesis, long timescales of evolution, and poor sampling of the true environmental diversity of photosynthetic bacteria. Here, we reconsider longstanding hypotheses for the evolutionary history of phototrophy by leveraging recent advances in metagenomic sequencing and phylogenetics to analyze relationships among phototrophic organisms and components of their photosynthesis pathways, including reaction centers and individual proteins and complexes involved in the multi-step synthesis of (bacterio)-chlorophyll pigments. We demonstrate that components of the photosynthetic apparatus have undergone extensive, independent histories of horizontal gene transfer. This suggests an evolutionary mode by which modular components of phototrophy are exchanged between diverse taxa in a piecemeal process that has led to biochemical innovation. We hypothesize that the evolution of extant anoxygenic photosynthetic bacteria has been spurred by ecological competition and restricted niches following the evolution of oxygenic Cyanobacteria and the accumulation of O2 in the atmosphere, leading to the relatively late evolution of bacteriochlorophyll pigments and the radiation of diverse crown group anoxygenic phototrophs. This hypothesis expands on the classic “Granick hypothesis” for the stepwise evolution of biochemical pathways, synthesizing recent expansion in our understanding of the diversity of phototrophic organisms as well as their evolving ecological context through Earth history.

Download Full-text

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).

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

UNIQUENESS, INTRACTABILITY AND EXACT ALGORITHMS: REFLECTIONS ON LEVEL-K PHYLOGENETIC NETWORKS

Journal of Bioinformatics and Computational Biology ◽

10.1142/s0219720009004308 ◽

2009 ◽

Vol 07 (04) ◽

pp. 597-623 ◽

Cited By ~ 26

Author(s):

LEO VAN IERSEL ◽

STEVEN KELK ◽

MATTHIAS MNICH

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Phylogenetic Trees ◽

Exact Algorithm ◽

Exact Algorithms ◽

Phylogenetic Networks ◽

Np Hard ◽

Level 1

Phylogenetic networks provide a way to describe and visualize evolutionary histories that have undergone so-called reticulate evolutionary events such as recombination, hybridization or horizontal gene transfer. The level k of a network determines how non-treelike the evolution can be, with level-0 networks being trees. We study the problem of constructing level-k phylogenetic networks from triplets, i.e. phylogenetic trees for three leaves (taxa). We give, for each k, a level-k network that is uniquely defined by its triplets. We demonstrate the applicability of this result by using it to prove that (1) for all k ≥ 1 it is NP-hard to construct a level-k network consistent with all input triplets, and (2) for all k ≥ 0 it is NP-hard to construct a level-k network consistent with a maximum number of input triplets, even when the input is dense. As a response to this intractability, we give an exact algorithm for constructing level-1 networks consistent with a maximum number of input triplets.

Download Full-text

Horizontal Transfer of Bacterial Cytolethal Distending Toxin B Genes to Insects

Molecular Biology and Evolution ◽

10.1093/molbev/msz146 ◽

2019 ◽

Vol 36 (10) ◽

pp. 2105-2110 ◽

Cited By ~ 2

Author(s):

Kirsten I Verster ◽

Jennifer H Wisecaver ◽

Marianthi Karageorgi ◽

Rebecca P Duncan ◽

Andrew D Gloss ◽

...

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Natural Enemies ◽

Larval Stage ◽

Horizontal Transfer ◽

Parasitoid Wasps ◽

Cytolethal Distending Toxin ◽

Toxin B ◽

Genes Encoding ◽

Hamiltonella Defensa

Abstract Horizontal gene transfer events have played a major role in the evolution of microbial species, but their importance in animals is less clear. Here, we report horizontal gene transfer of cytolethal distending toxin B (cdtB), prokaryotic genes encoding eukaryote-targeting DNase I toxins, into the genomes of vinegar flies (Diptera: Drosophilidae) and aphids (Hemiptera: Aphididae). We found insect-encoded cdtB genes are most closely related to orthologs from bacteriophage that infect Candidatus Hamiltonella defensa, a bacterial mutualistic symbiont of aphids that confers resistance to parasitoid wasps. In drosophilids, cdtB orthologs are highly expressed during the parasitoid-prone larval stage and encode a protein with ancestral DNase activity. We show that cdtB has been domesticated by diverse insects and hypothesize that it functions in defense against their natural enemies.

Download Full-text

Horizontal gene transfer: essentiality and evolvability in prokaryotes, and roles in evolutionary transitions

F1000Research ◽

10.12688/f1000research.8737.1 ◽

2016 ◽

Vol 5 ◽

pp. 1805 ◽

Cited By ~ 81

Author(s):

Eugene V. Koonin

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Phylogenetic Trees ◽

Point Mutations ◽

Theoretical Models ◽

Microbial Evolution ◽

Gene Gain ◽

Gene Trees ◽

Ratchet Effect ◽

Evolutionary Transitions

The wide spread of gene exchange and loss in the prokaryotic world has prompted the concept of ‘lateral genomics’ to the point of an outright denial of the relevance of phylogenetic trees for evolution. However, the pronounced coherence congruence of the topologies of numerous gene trees, particularly those for (nearly) universal genes, translates into the notion of a statistical tree of life (STOL), which reflects a central trend of vertical evolution. The STOL can be employed as a framework for reconstruction of the evolutionary processes in the prokaryotic world. Quantitatively, however, horizontal gene transfer (HGT) dominates microbial evolution, with the rate of gene gain and loss being comparable to the rate of point mutations and much greater than the duplication rate. Theoretical models of evolution suggest that HGT is essential for the survival of microbial populations that otherwise deteriorate due to the Muller’s ratchet effect. Apparently, at least some bacteria and archaea evolved dedicated vehicles for gene transfer that evolved from selfish elements such as plasmids and viruses. Recent phylogenomic analyses suggest that episodes of massive HGT were pivotal for the emergence of major groups of organisms such as multiple archaeal phyla as well as eukaryotes. Similar analyses appear to indicate that, in addition to donating hundreds of genes to the emerging eukaryotic lineage, mitochondrial endosymbiosis severely curtailed HGT. These results shed new light on the routes of evolutionary transitions, but caution is due given the inherent uncertainty of deep phylogenies.

Download Full-text