The impact of horizontal gene transfer in shaping operons and protein interaction networks – direct evidence of preferential attachment

Background  

Despite the prevalence of horizontal gene transfer (HGT) in bacteria, to this date there were few studies on HGT in the context of gene expression, operons and protein-protein interactions. Using the recently available data set on the E. coli protein-protein interaction network, we sought to explore the impact of HGT on genome structure and protein networks.     

Horizontal gene transfer in an acid mine drainage microbial community

Background

Horizontal gene transfer (HGT) has been widely identified in complete prokaryotic genomes. However, the roles of HGT among members of a microbial community and in evolution remain largely unknown. With the emergence of metagenomics, it is nontrivial to investigate such horizontal flow of genetic materials among members in a microbial community from the natural environment. Because of the lack of suitable methods for metagenomics gene transfer detection, microorganisms from a low-complexity community acid mine drainage (AMD) with near-complete genomes were used to detect possible gene transfer events and suggest the biological significance.

Results

Using the annotation of coding regions by the current tools, a phylogenetic approach, and an approximately unbiased test, we found that HGTs in AMD organisms are not rare, and we predicted 119 putative transferred genes. Among them, 14 HGT events were determined to be transfer events among the AMD members. Further analysis of the 14 transferred genes revealed that the HGT events affected the functional evolution of archaea or bacteria in AMD, and it probably shaped the community structure, such as the dominance of G-plasma in archaea in AMD through HGT.

Conclusions

Our study provides a novel insight into HGT events among microorganisms in natural communities. The interconnectedness between HGT and community evolution is essential to understand microbial community formation and development.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-015-1720-0) contains supplementary material, which is available to authorized users.     

Horizontal Gene Transfers in prokaryotes show differential preferences for metabolic and translational genes

Background  

Horizontal gene transfer (HGT) is an important process, which contributes in bacterial pathogenesis and drug resistance. A number of methods have been proposed for detection of horizontal gene transfer. One successful approach to the detection of HGT events is due to Novichkov et al. (J. Bacteriology 186, 6575–85), who rely on comparing phylogenetic distances within a gene family with genomic distances of the source organisms. Building on their approach, we introduce outlier detection in the correlation between those two sets of distances. This approach is designed to detect horizontal transfers of core set of genes present in many bacteria. The principle behind method allows detection of xenologous gene displacements as well as acquisition of novel genes.     

Exploring the evolutionary dynamics of plasmids: the <Emphasis Type="Italic">Acinetobacter</Emphasis> pan-plasmidome

Background  

Prokaryotic plasmids have a dual importance in the microbial world: first they have a great impact on the metabolic functions of the host cell, providing additional traits that can be accumulated in the cell without altering the gene content of the bacterial chromosome. Additionally and/or alternatively, from a genome perspective, plasmids can provide a basis for genomic rearrangements via homologous recombination and so they can facilitate the loss or acquisition of genes during these events, which eventually may lead to horizontal gene transfer (HGT). Given their importance for conferring adaptive traits to the host organisms, the interest in plasmid sequencing is growing and now many complete plasmid sequences are available online.     

HGTector: an automated method facilitating genome-wide discovery of putative horizontal gene transfers

Background

First pass methods based on BLAST match are commonly used as an initial step to separate the different phylogenetic histories of genes in microbial genomes, and target putative horizontal gene transfer (HGT) events. This will continue to be necessary given the rapid growth of genomic data and the technical difficulties in conducting large-scale explicit phylogenetic analyses. However, these methods often produce misleading results due to their inability to resolve indirect phylogenetic links and their vulnerability to stochastic events.

Results

A new computational method of rapid, exhaustive and genome-wide detection of HGT was developed, featuring the systematic analysis of BLAST hit distribution patterns in the context of a priori defined hierarchical evolutionary categories. Genes that fall beyond a series of statistically determined thresholds are identified as not adhering to the typical vertical history of the organisms in question, but instead having a putative horizontal origin. Tests on simulated genomic data suggest that this approach effectively targets atypically distributed genes that are highly likely to be HGT-derived, and exhibits robust performance compared to conventional BLAST-based approaches. This method was further tested on real genomic datasets, including Rickettsia genomes, and was compared to previous studies. Results show consistency with currently employed categories of HGT prediction methods. In-depth analysis of both simulated and real genomic data suggests that the method is notably insensitive to stochastic events such as gene loss, rate variation and database error, which are common challenges to the current methodology. An automated pipeline was created to implement this approach and was made publicly available at: https://github.com/DittmarLab/HGTector. The program is versatile, easily deployed, has a low requirement for computational resources.

Conclusions

HGTector is an effective tool for initial or standalone large-scale discovery of candidate HGT-derived genes.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-717) contains supplementary material, which is available to authorized users.     

An exceptional horizontal gene transfer in plastids: gene replacement by a distant bacterial paralog and evidence that haptophyte and cryptophyte plastids are sisters

Background  

Horizontal gene transfer (HGT) to the plant mitochondrial genome has recently been shown to occur at a surprisingly high rate; however, little evidence has been found for HGT to the plastid genome, despite extensive sequencing. In this study, we analyzed all genes from sequenced plastid genomes to unearth any neglected cases of HGT and to obtain a measure of the overall extent of HGT to the plastid.     

Bootstrap, Bayesian probability and maximum likelihood mapping: exploring new tools for comparative genome analyses

Background  

Horizontal gene transfer (HGT) played an important role in shaping microbial genomes. In addition to genes under sporadic selection, HGT also affects housekeeping genes and those involved in information processing, even ribosomal RNA encoding genes. Here we describe tools that provide an assessment and graphic illustration of the mosaic nature of microbial genomes.     

The cytoplasmic structure hypothesis for ribosome assembly,vertical inheritance,and phylogeny

Fundamental questions in evolution concern deep divisions in the living world and vertical versus horizontal information transfer. Two contrasting views are: (i) three superkingdoms Archaea, Eubacteria, and Eukarya based on vertical inheritance of genes encoding ribosomes; versus (ii) a prokaryotic/eukaryotic dichotomy with unconstrained horizontal gene transfer (HGT) among prokaryotes. Vertical inheritance implies continuity of cytoplasmic and structural information whereas HGT transfers only DNA. By hypothesis, HGT of the translation machinery is constrained by interaction between new ribosomal gene products and vertically inherited cytoplasmic structure made largely of preexisting ribosomes. Ribosomes differentially enhance the assembly of new ribosomes made from closely related genes and inhibit the assembly of products from more distal genes. This hypothesis suggests experiments for synthetic biology: the ability of synthetic genomes to “boot,” i.e., establish hereditary continuity, will be constrained by the phylogenetic closeness of the cell “body” into which genomes are placed.     

The ancestor of the <Emphasis Type="Italic">Paulinella</Emphasis> chromatophore obtained a carboxysomal operon by horizontal gene transfer from a <Emphasis Type="Italic">Nitrococcus</Emphasis>-like γ-proteobacterium

Background  

Paulinella chromatophora is a freshwater filose amoeba with photosynthetic endosymbionts (chromatophores) of cyanobacterial origin that are closely related to free-living Prochlorococcus and Synechococcus species (PS-clade). Members of the PS-clade of cyanobacteria contain a proteobacterial form 1A RubisCO (ribulose-1,5-bisphosphate carboxylase/oxygenase) that was acquired by horizontal gene transfer (HGT) of a carboxysomal operon. In rDNA-phylogenies, the Paulinella chromatophore diverged basal to the PS-clade, raising the question whether the HGT occurred before or after the split of the chromatophore ancestor.     

Variation suggestive of horizontal gene transfer at a lipopolysaccharide (<Emphasis Type="Italic">lps</Emphasis>) biosynthetic locus in <Emphasis Type="Italic">Xanthomonas oryzae</Emphasis> pv. <Emphasis Type="Italic">oryzae</Emphasis>, the bacterial leaf blight pathogen of rice

Background  

In animal pathogenic bacteria, horizontal gene transfer events (HGT) have been frequently observed in genomic regions that encode functions involved in biosynthesis of the outer membrane located lipopolysaccharide (LPS). As a result, different strains of the same pathogen can have substantially different lps biosynthetic gene clusters. Since LPS is highly antigenic, the variation at lps loci is attributed to be of advantage in evading the host immune system. Although LPS has been suggested as a potentiator of plant defense responses, interstrain variation at lps biosynthetic gene clusters has not been reported for any plant pathogenic bacterium.     

Phylogenetic detection of horizontal gene transfer during the step-wise genesis of Mycobacterium tuberculosis

Background  

In the past decade, the availability of complete genome sequence data has greatly facilitated comparative genomic research aimed at addressing genetic variability within species. More recently, analysis across species has become feasible, especially in genera where genome sequencing projects of multiple species have been initiated. To understand the genesis of the pathogen Mycobacterium tuberculosis within a genus where the majority of species are harmless environmental organisms, we have used genome sequence data from 16 mycobacteria to look for evidence of horizontal gene transfer (HGT) associated with the emergence of pathogenesis. First, using multi-locus sequence analysis (MLSA) of 20 housekeeping genes across these species, we derived a phylogeny that serves as the basis for HGT assignments. Next, we performed alignment searches for the 3989 proteins of M. tuberculosis H37Rv against 15 other mycobacterial genomes, generating a matrix of 59835 comparisons, to look for genetic elements that were uniquely found in M. tuberculosis and closely-related pathogenic mycobacteria. To assign when foreign genes were likely acquired, we designed a bioinformatic program called mycoHIT (mycobacterial homologue investigation tool) to analyze these data in conjunction with the MLSA-based phylogeny.     

Identification of horizontally transferred genes in the genus Colletotrichum reveals a steady tempo of bacterial to fungal gene transfer

Background

Horizontal gene transfer (HGT) is the stable transmission of genetic material between organisms by means other than vertical inheritance. HGT has an important role in the evolution of prokaryotes but is relatively rare in eukaryotes. HGT has been shown to contribute to virulence in eukaryotic pathogens. We studied the importance of HGT in plant pathogenic fungi by identifying horizontally transferred genes in the genomes of three members of the genus Colletotrichum.

Results

We identified eleven HGT events from bacteria into members of the genus Colletotrichum or their ancestors. The HGT events include genes involved in amino acid, lipid and sugar metabolism as well as lytic enzymes. Additionally, the putative minimal dates of transference were calculated using a time calibrated phylogenetic tree. This analysis reveals a constant flux of genes from bacteria to fungi throughout the evolution of subphylum Pezizomycotina.

Conclusions

Genes that are typically transferred by HGT are those that are constantly subject to gene duplication and gene loss. The functions of some of these genes suggest roles in niche adaptation and virulence. We found no evidence of a burst of HGT events coinciding with major geological events. In contrast, HGT appears to be a constant, albeit rare phenomenon in the Pezizomycotina, occurring at a steady rate during their evolution.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-16-2) contains supplementary material, which is available to authorized users.     

Score-based prediction of genomic islands in prokaryotic genomes using hidden Markov models

Background  

Horizontal gene transfer (HGT) is considered a strong evolutionary force shaping the content of microbial genomes in a substantial manner. It is the difference in speed enabling the rapid adaptation to changing environmental demands that distinguishes HGT from gene genesis, duplications or mutations. For a precise characterization, algorithms are needed that identify transfer events with high reliability. Frequently, the transferred pieces of DNA have a considerable length, comprise several genes and are called genomic islands (GIs) or more specifically pathogenicity or symbiotic islands.     

Extensive Intra-Kingdom Horizontal Gene Transfer Converging on a Fungal Fructose Transporter Gene

Comparative genomics revealed in the last decade a scenario of rampant horizontal gene transfer (HGT) among prokaryotes, but for fungi a clearly dominant pattern of vertical inheritance still stands, punctuated however by an increasing number of exceptions. In the present work, we studied the phylogenetic distribution and pattern of inheritance of a fungal gene encoding a fructose transporter (FSY1) with unique substrate selectivity. 109 FSY1 homologues were identified in two sub-phyla of the Ascomycota, in a survey that included 241 available fungal genomes. At least 10 independent inter-species instances of horizontal gene transfer (HGT) involving FSY1 were identified, supported by strong phylogenetic evidence and synteny analyses. The acquisition of FSY1 through HGT was sometimes suggestive of xenolog gene displacement, but several cases of pseudoparalogy were also uncovered. Moreover, evidence was found for successive HGT events, possibly including those responsible for transmission of the gene among yeast lineages. These occurrences do not seem to be driven by functional diversification of the Fsy1 proteins because Fsy1 homologues from widely distant lineages, including at least one acquired by HGT, appear to have similar biochemical properties. In summary, retracing the evolutionary path of the FSY1 gene brought to light an unparalleled number of independent HGT events involving a single fungal gene. We propose that the turbulent evolutionary history of the gene may be linked to the unique biochemical properties of the encoded transporter, whose predictable effect on fitness may be highly variable. In general, our results support the most recent views suggesting that inter-species HGT may have contributed much more substantially to shape fungal genomes than heretofore assumed.     

Horizontal gene transfer in chromalveolates

Background  

Horizontal gene transfer (HGT), the non-genealogical transfer of genetic material between different organisms, is considered a potentially important mechanism of genome evolution in eukaryotes. Using phylogenomic analyses of expressed sequence tag (EST) data generated from a clonal cell line of a free living dinoflagellate alga Karenia brevis, we investigated the impact of HGT on genome evolution in unicellular chromalveolate protists.     

Interkingdom protein domain fusion: the case of an antimicrobial protein in potato (Solanum tuberosum)

Horizontal gene transfer (HGT) is thought to have been involved in both prokaryotic and eukaryotic evolution. However, the extent to which it shapes eukaryotic genomes is still questionable. The ability to detect and study horizontal gene transfer events is of significant importance to our understanding of its effect on the evolution of eukaryotic genes and genomes. We performed phylogenetic analysis of a published anti-bacterial protein AP1 from potato (Solanum tuberosum). One domain encodes a phosphoesterase with high similarity to an acid phosphatase of Ralstonia solanacearum and closely related Betaproteobacteria. The second domain encodes an UspA-like domain similar to those present in plants. Our phylogenetic analyses suggest that both domains evolved along different evolutionary pathways until they merged into a single gene. We propose that the phosphoesterase domain was acquired by HGT. Our results support claims in favor of HGT detection at the protein domain level. The case of anti-bacterial protein AP1 in potato highlights the significance of gene fusion/protein domain fusion as an important feature of horizontal gene transfer which may contribute substantially to the adaptive abilities of eukaryotic organisms.     

Horizontal acquisition of multiple mitochondrial genes from a parasitic plant followed by gene conversion with host mitochondrial genes

Background  

Horizontal gene transfer (HGT) is relatively common in plant mitochondrial genomes but the mechanisms, extent and consequences of transfer remain largely unknown. Previous results indicate that parasitic plants are often involved as either transfer donors or recipients, suggesting that direct contact between parasite and host facilitates genetic transfer among plants.     

Ribonucleotide reduction - horizontal transfer of a required function spans all three domains

Background  

Ribonucleotide reduction is the only de novo pathway for synthesis of deoxyribonucleotides, the building blocks of DNA. The reaction is catalysed by ribonucleotide reductases (RNRs), an ancient enzyme family comprised of three classes. Each class has distinct operational constraints, and are broadly distributed across organisms from all three domains, though few class I RNRs have been identified in archaeal genomes, and classes II and III likewise appear rare across eukaryotes. In this study, we examine whether this distribution is best explained by presence of all three classes in the Last Universal Common Ancestor (LUCA), or by horizontal gene transfer (HGT) of RNR genes. We also examine to what extent environmental factors may have impacted the distribution of RNR classes.     

Systematic Detection of Large-Scale Multigene Horizontal Transfer in Prokaryotes

Horizontal gene transfer (HGT) is central to prokaryotic evolution. However, little is known about the “scale” of individual HGT events. In this work, we introduce the first computational framework to help answer the following fundamental question: How often does more than one gene get horizontally transferred in a single HGT event? Our method, called HoMer, uses phylogenetic reconciliation to infer single-gene HGT events across a given set of species/strains, employs several techniques to account for inference error and uncertainty, combines that information with gene order information from extant genomes, and uses statistical analysis to identify candidate horizontal multigene transfers (HMGTs) in both extant and ancestral species/strains. HoMer is highly scalable and can be easily used to infer HMGTs across hundreds of genomes. We apply HoMer to a genome-scale data set of over 22,000 gene families from 103 Aeromonas genomes and identify a large number of plausible HMGTs of various scales at both small and large phylogenetic distances. Analysis of these HMGTs reveals interesting relationships between gene function, phylogenetic distance, and frequency of multigene transfer. Among other insights, we find that 1) the observed relative frequency of HMGT increases as divergence between genomes increases, 2) HMGTs often have conserved gene functions, and 3) rare genes are frequently acquired through HMGT. We also analyze in detail HMGTs involving the zonula occludens toxin and type III secretion systems. By enabling the systematic inference of HMGTs on a large scale, HoMer will facilitate a more accurate and more complete understanding of HGT and microbial evolution.