Estimating the Frequency of Horizontal Gene Transfer Using Phylogenetic Models of Gene Gain and Loss

Abstract High-throughput shotgun metagenomics sequencing has enabled the profiling of myriad natural communities. These data are commonly used to identify gene families and pathways that were potentially gained or lost in an environment and which may be involved in microbial adaptation. Despite the widespread interest in these events, there are no established best practices for identifying gene gain and loss in metagenomics data. Horizontal gene transfer (HGT) represents several mechanisms of gene gain that are especially of interest in clinical microbiology due to the rapid spread of antibiotic resistance genes in natural communities. Several additional mechanisms of gene gain and loss, including gene duplication, gene loss-of-function events, and de novo gene birth are also important to consider in the context of metagenomes but have been less studied. This review is largely focused on detecting HGT in prokaryotic metagenomes, but methods for detecting these other mechanisms are first discussed. For this article to be self-contained, we provide a general background on HGT and the different possible signatures of this process. Lastly, we discuss how improved assembly of genomes from metagenomes would be the most straight-forward approach for improving the inference of gene gain and loss events. Several recent technological advances could help improve metagenome assemblies: long-read sequencing, determining the physical proximity of contigs, optical mapping of short sequences along chromosomes, and single-cell metagenomics. The benefits and limitations of these advances are discussed and open questions in this area are highlighted.

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Plasmids Related to the Symbiotic Nitrogen Fixation Are Not Only Cooperated Functionally but Also May Have Evolved over a Time Span in Family Rhizobiaceae

Genome Biology and Evolution ◽

10.1093/gbe/evaa152 ◽

2020 ◽

Vol 12 (11) ◽

pp. 2002-2014

Author(s):

Ling-Ling Yang ◽

Zhao Jiang ◽

Yan Li ◽

En-Tao Wang ◽

Xiao-Yang Zhi

Keyword(s):

Nitrogen Fixation ◽

Gene Transfer ◽

Horizontal Gene Transfer ◽

Symbiotic Nitrogen Fixation ◽

Gene Families ◽

Time Span ◽

Soil Conditions ◽

Gene Gain ◽

Nitrogen Fixing ◽

Pan Genome

Abstract Rhizobia are soil bacteria capable of forming symbiotic nitrogen-fixing nodules associated with leguminous plants. In fast-growing legume-nodulating rhizobia, such as the species in the family Rhizobiaceae, the symbiotic plasmid is the main genetic basis for nitrogen-fixing symbiosis, and is susceptible to horizontal gene transfer. To further understand the symbioses evolution in Rhizobiaceae, we analyzed the pan-genome of this family based on 92 genomes of type/reference strains and reconstructed its phylogeny using a phylogenomics approach. Intriguingly, although the genetic expansion that occurred in chromosomal regions was the main reason for the high proportion of low-frequency flexible gene families in the pan-genome, gene gain events associated with accessory plasmids introduced more genes into the genomes of nitrogen-fixing species. For symbiotic plasmids, although horizontal gene transfer frequently occurred, transfer may be impeded by, such as, the host’s physical isolation and soil conditions, even among phylogenetically close species. During coevolution with leguminous hosts, the plasmid system, including accessory and symbiotic plasmids, may have evolved over a time span, and provided rhizobial species with the ability to adapt to various environmental conditions and helped them achieve nitrogen fixation. These findings provide new insights into the phylogeny of Rhizobiaceae and advance our understanding of the evolution of symbiotic nitrogen fixation.

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Shared transcriptional control and disparate gain and loss of aphid parasitism genes and loci acquired via horizontal gene transfer

10.1101/246801 ◽

2018 ◽

Cited By ~ 5

Author(s):

Peter Thorpe ◽

Carmen M. Escudero-Martinez ◽

Peter J. A. Cock ◽

D. Laetsch ◽

Sebastian Eves-van den Akker ◽

...

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Gene Duplication ◽

Host Range ◽

Genome Evolution ◽

Transcriptional Control ◽

Control Mechanism ◽

Aphid Species ◽

Gain And Loss ◽

Genome Assemblies

AbstractBackgroundAphids are a diverse group of taxa that contain hundreds of agronomically important species, which vary in their host range and pathogenicity. However, the genome evolution underlying agriculturally important aphid traits is not well understood.ResultsWe generated highly-contiguous draft genome assemblies for two aphid species: the narrow host range Myzus cerasi, and the cereal specialist Rhopalosiphum padi. Using a de novo gene prediction pipeline on both these genome assemblies, and those of three related species (Acyrthosiphon pisum, D. noxia and M. persicae), we show that aphid genomes consistently encode similar gene numbers, and in the case of A. pisum, fewer and larger genes than previously reported. We compare gene content, gene duplication, synteny, horizontal gene transfer events, and putative effector repertoires between these five species to understand the genome evolution of globally important plant parasites.Aphid genomes show signs of relatively distant gene duplication, and substantial, relatively recent, gene birth, and are characterized by disparate gain and loss of genes acquired by horizontal gene transfer (HGT). Such HGT events account for approximately 1% of loci, and contribute to the protein-coding content of aphid species analysed. Putative effector repertoires, originating from duplicated loci, putative HGT events and other loci, have an unusual genomic organisation and evolutionary history. We identify a highly conserved effector-pair that is tightly genetically-linked in all aphid species. In R. padi, this effector pair is tightly transcriptionally-linked, and shares a transcriptional control mechanism with a subset of approximately 50 other putative effectors distributed across the genome.ConclusionsThis study extends our current knowledge on the evolution of aphid genomes and reveals evidence for a shared control mechanism, which underlies effector expression, and ultimately plant parasitism.

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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.

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Horizontal gene transfer drives the evolution of dependencies in bacteria

10.1101/836403 ◽

2019 ◽

Author(s):

Akshit Goyal

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Metabolic Networks ◽

Gene Loss ◽

Bacterial Species ◽

Gene Gain ◽

Metabolic Interactions ◽

Gain Loss ◽

Gains And Losses ◽

The Impact

Many naturally-occurring bacteria lead a lifestyle of metabolic dependency, i.e., they depend on others for crucial resources. We do not understand what factors drive bacteria towards this lifestyle, and how. Here, we systematically show that horizontal gene transfer (HGT) plays a crucial role in the evolution of dependencies in bacteria. Across 835 bacterial species, we map gene gain-loss dynamics on a deep evolutionary tree, and assess the impact of HGT and gene loss on bacterial metabolic networks. Our analyses suggest that genes acquired by HGT can affect which genes are later lost. Dependency evolution is contingent on earlier HGT because of two reasons. First, we find that HGT typically adds new catabolic routes to bacterial metabolic networks. This increases the chance of new metabolic interactions between bacteria, which is a prerequisite for dependency evolution. Second, we show that gaining new routes can promote the loss of specific ancestral routes (a mechanism we call “coupled gains and losses”, CGLs). Phylogenetic patterns indicate that both types of dependencies — those mediated by CGLs and those purely by gene loss — are equally likely. Our results highlight HGT as an important driver of metabolic dependency evolution in bacteria.

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Deciphering Functional Redundancy in the Human Microbiome

10.1101/176313 ◽

2017 ◽

Cited By ~ 6

Author(s):

Liang Tian ◽

Xu-Wen Wang ◽

Ang-Kun Wu ◽

Yuhang Fan ◽

Jonathan Friedman ◽

...

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Degree Distribution ◽

Selection Pressure ◽

Human Microbiome ◽

Functional Redundancy ◽

Taxonomic Composition ◽

Gene Gain ◽

Topological Features ◽

Nested Structure

Although the taxonomic composition of the human microbiome varies tremendously across individuals, its gene composition or functional capacity is highly conserved1-5---implying an ecological property known as functional redundancy. Such functional redundancy is thought to underlie the stability and resilience of the human microbiome6,7, but its origin is elusive. Here, we investigate the basis for functional redundancy in the human microbiome by analyzing its genomic content network --- a bipartite graph that links microbes to the genes in their genomes. We show that this network exhibits several topological features, such as highly nested structure and fat-tailed gene degree distribution, which favor high functional redundancy. To explain the origins of these topological features, we develop a simple genome evolution model that explicitly considers selection pressure, and the processes of gene gain and loss, and horizontal gene transfer. We find that moderate selection pressure and high horizontal gene transfer rate are necessary to generate genomic content networks with both highly nested structure and fat-tailed gene degree distribution, and consequently favor high functional redundancy. These findings provide insights into the relationships between structure and function in complex microbial communities. This work elucidates the potential ecological and evolutionary processes that create and maintain functional redundancy in the human microbiome and contribute to its resilience.

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

10.1101/684704 ◽

2019 ◽

Author(s):

Daniela Sánchez-Soto ◽

Guillermin Agüero-Chapin ◽

Vinicio Armijos-Jaramillo ◽

Yunierkis Perez-Castillo ◽

Eduardo Tejera ◽

...

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Hybrid Approach ◽

Phylogenetic Reconstruction ◽

Heavy Metal Resistance ◽

Metal Resistance ◽

Computational Approaches ◽

Link Type ◽

Reconstruction Methods ◽

Phylogenetic Models

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/.

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