Horizontal gene transfer in human-associated microorganisms inferred by phylogenetic reconstruction and reconciliation.
ABSTRACT: Horizontal gene transfer (HGT) is widespread in the evolution of prokaryotes, especially those associated with the human body. Here, we implemented large-scale gene-species phylogenetic tree reconstructions and reconciliations to identify putative HGT-derived genes in the reference genomes of microbiota isolated from six major human body sites by the NIH Human Microbiome Project. Comparisons with a control group representing microbial genomes from diverse natural environments indicated that HGT activity increased significantly in the genomes of human microbiota, which is confirmatory of previous findings. Roughly, more than half of total genes in the genomes of human-associated microbiota were transferred (donated or received) by HGT. Up to 60% of the detected HGTs occurred either prior to the colonization of the human body or involved bacteria residing in different body sites. The latter could suggest 'genetic crosstalk' and movement of bacterial genes within the human body via hitherto poorly understood mechanisms. We also observed that HGT activity increased significantly among closely-related microorganisms and especially when they were united by physical proximity, suggesting that the 'phylogenetic effect' can significantly boost HGT activity. Finally, we identified several core and widespread genes least influenced by HGT that could become useful markers for building robust 'trees of life' and address several outstanding technical challenges to improve the phylogeny-based genome-wide HGT detection method for future applications.
Project description:BACKGROUND: Horizontal gene transfer (HGT) is considered to be a major force driving the evolutionary history of prokaryotes. HGT is widespread in prokaryotes, contributing to the genomic repertoire of prokaryotic organisms, and is particularly apparent in Rickettsiales genomes. Gene gains from both distantly and closely related organisms play crucial roles in the evolution of bacterial genomes. In this work, we focus on genes transferred from distantly related species into Rickettsiales species. RESULTS: We developed an automated approach for the detection of HGT from other organisms (excluding alphaproteobacteria) into Rickettsiales genomes. Our systematic approach consisted of several specialized features including the application of a parsimony method for inferring phyletic patterns followed by blast filter, automated phylogenetic reconstruction and the application of patterns for HGT detection. We identified 42 instances of HGT in 31 complete Rickettsiales genomes, of which 38 were previously unidentified instances of HGT from Anaplasma, Wolbachia, Candidatus Pelagibacter ubique and Rickettsia genomes. Additionally, putative cases with no phylogenetic support were assigned gene ontology terms. Overall, these transfers could be characterized as "rhizome-like". CONCLUSIONS: Our analysis provides a comprehensive, systematic approach for the automated detection of HGTs from several complete proteome sequences that can be applied to detect instances of HGT within other genomes of interest.
Project description:Horizontal gene transfer (HGT) was attributed as a major driving force for the innovation and evolution of prokaryotic genomes. Previously, multiple research endeavors were undertaken to decipher HGT in different bacterial lineages. The genus Mycobacterium houses some of the most deadly human pathogens; however, the impact of HGT in Mycobacterium has never been addressed in a systematic way. Previous initiatives to explore the genomic imprints of HGTs in Mycobacterium were focused on few selected species, specifically among the members of Mycobacterium tuberculosis complex. Considering the recent availability of a large number of genomes, the current study was initiated to decipher the probable events of HGTs among 109 completely sequenced Mycobacterium species. Our comprehensive phylogenetic analysis with more than 9,000 families of Mycobacterium proteins allowed us to list several instances of gene transfers spread across the Mycobacterium phylogeny. Moreover, by examining the topology of gene phylogenies here, we identified the species most likely to donate and receive these genes and provided a detailed overview of the putative functions these genes may be involved in. Our study suggested that horizontally acquired foreign genes had played an enduring role in the evolution of Mycobacterium genomes and have contributed to their metabolic versatility and pathogenicity.
Project description:The prominent role of Horizontal Gene Transfer (HGT) in the evolution of bacteria is now well documented, but few studies have differentiated between evolutionary events that predominantly cause genes in one lineage to be replaced by homologs from another lineage ("replacing HGT") and events that result in the addition of substantial new genomic material ("additive HGT"). Here in, we make use of the distinct phylogenetic signatures of replacing and additive HGTs in a genome-wide study of the important human pathogen Streptococcus pyogenes (SPY) and its close relatives S. dysgalactiae subspecies equisimilis (SDE) and S. dysgalactiae subspecies dysgalactiae (SDD). Using recently developed statistical models and computational methods, we find evidence for abundant gene flow of both kinds within each of the SPY and SDE clades and of reduced levels of exchange between SPY and SDD. In addition, our analysis strongly supports a pronounced asymmetry in SPY-SDE gene flow, favoring the SPY-to-SDE direction. This finding is of particular interest in light of the recent increase in virulence of pathogenic SDE. We find much stronger evidence for SPY-SDE gene flow among replacing than among additive transfers, suggesting a primary influence from homologous recombination between co-occurring SPY and SDE cells in human hosts. Putative virulence genes are correlated with transfer events, but this correlation is found to be driven by additive, not replacing, HGTs. The genes affected by additive HGTs are enriched for functions having to do with transposition, recombination, and DNA integration, consistent with previous findings, whereas replacing HGTs seen to influence a more diverse set of genes. Additive transfers are also found to be associated with evidence of positive selection. These findings shed new light on the manner in which HGT has shaped pathogenic bacterial genomes.
Project description:The extent and role of horizontal gene transfer (HGT) in phytoplankton and, more broadly, eukaryotic evolution remain controversial topics. Recent studies substantiate the importance of HGT in modifying or expanding functions such as metal or reactive species detoxification and buttressing halotolerance. Yet, the potential of HGT to significantly alter the fate of species in a major eukaryotic assemblage remains to be established. We provide such an example for the ecologically important lineages encompassed by cryptophytes, rhizarians, alveolates, stramenopiles, and haptophytes ("CRASH" taxa). We describe robust evidence of prokaryotic HGTs in these taxa affecting functions such as polysaccharide biosynthesis. Numbers of HGTs range from 0.16 to 1.44% of CRASH species gene inventories, comparable to the ca. 1% prokaryote-derived HGTs found in the genomes of extremophilic red algae. Our results substantially expand the impact of HGT in eukaryotes and define a set of general principles for prokaryotic gene fixation in phytoplankton genomes.
Project description:BACKGROUND: Recent studies have shown that plant genomes have potentially undergone rampant horizontal gene transfer (HGT). In plant parasitic systems HGT appears to be facilitated by the intimate physical association between the parasite and its host. HGT in these systems has been invoked when a DNA sequence obtained from a parasite is placed phylogenetically very near to its host rather than with its closest relatives. Studies of HGT in parasitic plants have relied largely on the fortuitous discovery of gene phylogenies that indicate HGT, and no broad systematic search for HGT has been undertaken in parasitic systems where it is most expected to occur. RESULTS: We analyzed the transcriptomes of the holoparasite Rafflesia cantleyi Solms-Laubach and its obligate host Tetrastigma rafflesiae Miq. using phylogenomic approaches. Our analyses show that several dozen actively transcribed genes, most of which appear to be encoded in the nuclear genome, are likely of host origin. We also find that hundreds of vertically inherited genes (VGT) in this parasitic plant exhibit codon usage properties that are more similar to its host than to its closest relatives. CONCLUSIONS: Our results establish for the first time a substantive number of HGTs in a plant host-parasite system. The elevated rate of unidirectional host-to- parasite gene transfer raises the possibility that HGTs may provide a fitness benefit to Rafflesia for maintaining these genes. Finally, a similar convergence in codon usage of VGTs has been shown in microbes with high HGT rates, which may help to explain the increase of HGTs in these parasitic plants.
Project description:Many studies have reported horizontal gene transfer (HGT) events from eukaryotes, especially fungi. However, only a few investigations summarized multiple interkingdom HGTs involving important phytopathogenic species of Pyrenophora and few have investigated the genetic contributions of HGTs to fungi. We investigated HGT events in P. teres and P. tritici-repentis and discovered that both species harbored 14 HGT genes derived from bacteria and plants, including 12 HGT genes that occurred in both species. One gene coding a leucine-rich repeat protein was present in both species of Pyrenophora and it may have been transferred from a host plant. The transfer of genes from a host plant to pathogenic fungi has been reported rarely and we discovered the first evidence for this transfer in phytopathogenic Pyrenophora. Two HGTs in Pyrenophora underwent subsequent duplications. Some HGT genes had homologs in a few other fungi, indicating relatively ancient transfer events. Functional analyses indicated that half of the HGT genes encoded extracellular proteins and these may have facilitated the infection of plants by Pyrenophora via interference with plant defense-response and the degradation of plant cell walls. Some other HGT genes appeared to participate in carbohydrate metabolism. Together, these functions implied that HGTs may have led to highly efficient mechanisms of infection as well as the utilization of host carbohydrates. Evolutionary analyses indicated that HGT genes experienced amelioration, purifying selection, and accelerated evolution. These appeared to constitute adaptations to the background genome of the recipient. The discovery of multiple interkingdom HGTs in Pyrenophora, their significance to infection, and their adaptive evolution, provided valuable insights into the evolutionary significance of interkingdom HGTs from multiple donors.
Project description:BACKGROUND:Metagenomic datasets provide an opportunity to study horizontal gene transfer (HGT) on the level of a microbial community. However, current HGT detection methods cannot be applied to community-level datasets or require reference genomes. Here, we present MetaCHIP, a pipeline for reference-independent HGT identification at the community level. RESULTS:Assessment of MetaCHIP's performance on simulated datasets revealed that it can predict HGTs with various degrees of genetic divergence from metagenomic datasets. The results also indicated that the detection of very recent gene transfers (i.e. those with low levels of genetic divergence) from metagenomics datasets is largely affected by the read assembly step. Comparison of MetaCHIP with a previous analysis on soil bacteria showed a high level of consistency for the prediction of recent HGTs and revealed a large number of additional non-recent gene transfers, which can provide new biological and ecological insight. Assessment of MetaCHIP's performance on real metagenomic datasets confirmed the role of HGT in the spread of genes related to antibiotic resistance in the human gut microbiome. Further testing also showed that functions related to energy production and conversion as well as carbohydrate transport and metabolism are frequently transferred among free-living microorganisms. CONCLUSION:MetaCHIP provides an opportunity to study HGTs among members of a microbial community and therefore has several applications in the field of microbial ecology and evolution. MetaCHIP is implemented in Python and freely available at https://github.com/songweizhi/MetaCHIP .
Project description:Microsporidia are obligate intracellular parasites whose genomes have been shaped by an extreme lifestyle. Specifically, their obligate intracellular parasitism has resulted in the loss of many genes and biochemical pathways, but these reductive processes have been often offset by the acquisition of several genes by means of horizontal gene transfer (HGT). Until recently, these HGTs were all found to have derived from prokaryotic donors, but a recent study suggests that some species took advantage of this mechanism to acquire one gene from an animal, which they maintained in their genome for metabolic purposes. The gene encodes for a purine nucleoside phosphorylase, and shows a strong phylogenetic signal of arthropod origin. Here, we briefly review our current knowledge of HGTs discovered across microsporidian genomes and discuss the implications of the most recent findings in this research area for understanding the origin and evolution of this highly adapted group of intracellular parasites. A novel gene potentially transferred by means of HGT to one microsporidia is also reported.
Project description:Horizontal gene transfer (HGT) can radically alter the genomes of microorganisms, providing the capacity to adapt to new lifestyles, environments, and hosts. However, the extent of HGT between eukaryotes is unclear. Using whole-genome, gene-by-gene phylogenetic analysis we demonstrate an extensive pattern of cross-kingdom HGT between fungi and oomycetes. Comparative genomics, including the de novo genome sequence of Hyphochytrium catenoides, a free-living sister of the oomycetes, shows that these transfers largely converge within the radiation of oomycetes that colonize plant tissues. The repertoire of HGTs includes a large number of putatively secreted proteins; for example, 7.6% of the secreted proteome of the sudden oak death parasite Phytophthora ramorum has been acquired from fungi by HGT. Transfers include gene products with the capacity to break down plant cell walls and acquire sugars, nucleic acids, nitrogen, and phosphate sources from the environment. Predicted HGTs also include proteins implicated in resisting plant defense mechanisms and effector proteins for attacking plant cells. These data are consistent with the hypothesis that some oomycetes became successful plant parasites by multiple acquisitions of genes from fungi.
Project description:BACKGROUND:Horizontal Gene Transfer (HGT) refers to the transfer of genetic materials between organisms through mechanisms other than parent-offspring inheritance. HGTs may affect human health through a large number of microorganisms, especially the gut microbiomes which the human body harbors. The transferred segments may lead to complicated local genome structural variations. Details of the local genome structure can elucidate the effects of the HGTs. RESULTS:In this work, we propose a graph-based method to reconstruct the local strains from the gut metagenomics data at the HGT sites. The method is implemented in a package named LEMON. The simulated results indicate that the method can identify transferred segments accurately on reference sequences of the microbiome. Simulation results illustrate that LEMON could recover local strains with complicated structure variation. Furthermore, the gene fusion points detected in real data near HGT breakpoints validate the accuracy of LEMON. Some strains reconstructed by LEMON have a replication time profile with lower standard error, which demonstrates HGT events recovered by LEMON is reliable. CONCLUSIONS:Through LEMON we could reconstruct the sequence structure of bacteria, which harbors HGT events. This helps us to study gene flow among different microbial species.