Uncovering rate variation of lateral gene transfer during bacterial genome evolution
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ABSTRACT:
SUBMITTER: Hao W
PROVIDER: S-EPMC2628915 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:BackgroundLarge scale genome arrangement, such as whole gene insertion/deletion, plays an important role in bacterial genome evolution. Various methods have been employed to study the dynamic process of gene insertions and deletions, such as parsimony methods and maximum likelihood methods. Previous maximum likelihood studies have assumed that the rate of gene insertions/deletions is constant over different genes. This assumption is unrealistic. For instance, it has been shown that informational genes are less likely to be laterally transferred than non-informational genes. However, how much of the variation in gene transfer rates is due to the difference between informational genes and non-informational genes is unclear. In this study, a Gamma-distribution was incorporated in the likelihood estimation by considering rate variation for gene insertions/deletions between genes. This makes it possible to address whether a difference between informational genes and non-informational genes is the main contributor to rate variation of lateral gene transfers.ResultsThe results show that models incorporating rate variation fit the data better than do constant rate models in many phylogenetic groups. Even though informational genes are less likely to be laterally transferred than non-informational genes, the degree of rate variation for insertions/deletions did not change dramatically and remained high even when informational genes were excluded from the study. This suggests that the variation in rate of insertions/deletions is not due mainly to the simple difference between informational genes and non-informational genes. Among genes that are not classified as informational and among the informational genes themselves, there are still large differences in the rates that these genes are inserted and deleted.ConclusionWhile the difference in informational gene rates contributes to rate variation, it is only a small fraction of the variation present; instead, a substantial amount of rate variation for insertions/deletions remains among both informational genes and among non-informational genes.
| S-EPMC2426709 | biostudies-literature
Project description:The amount of lateral gene transfer (LGT) that has occurred in microbial evolution is heavily debated. Efforts to quantify LGT through gene-tree comparisons have delivered estimates that between 2% and 60% of all prokaryotic genes have been affected by LGT, the 30-fold discrepancy reflecting differences among gene samples studied and uncertainties inherent in phylogenetic reconstruction. Here we present a simple method that is independent of gene-tree comparisons to estimate the LGT rate among sequenced prokaryotic genomes. If little or no LGT has occurred during evolution, ancestral genome sizes would become unrealistically large, whereas too much LGT would render them far too small. We determine the amount of LGT that is necessary and sufficient to bring the distribution of inferred ancestral genome sizes into agreement with that observed among modern microbes. Rather than testing for phylogenetic congruence or lack thereof across genes, we assume that all gene trees are compatible; hence, our method delivers very conservative lower-bound estimates of the average LGT rate. The results indicate that among 57,670 gene families distributed across 190 sequenced genomes, at least two-thirds and probably all, have been affected by LGT at some time in their evolutionary past. A component of common ancestry nonetheless remains detectable in gene distribution patterns. We estimate the minimum lower bound for the average LGT rate across all genes as 1.1 LGT events per gene family and gene family lifespan and this minimum rate increases sharply when genes present in only a few genomes are excluded from the analysis.
| S-EPMC1783406 | biostudies-literature
Project description:Like biological species, languages change over time. As noted by Darwin, there are many parallels between language evolution and biological evolution. Insights into these parallels have also undergone change in the past 150 years. Just like genes, words change over time, and language evolution can be likened to genome evolution accordingly, but what kind of evolution? There are fundamental differences between eukaryotic and prokaryotic evolution. In the former, natural variation entails the gradual accumulation of minor mutations in alleles. In the latter, lateral gene transfer is an integral mechanism of natural variation. The study of language evolution using biological methods has attracted much interest of late, most approaches focusing on language tree construction. These approaches may underestimate the important role that borrowing plays in language evolution. Network approaches that were originally designed to study lateral gene transfer may provide more realistic insights into the complexities of language evolution.
| S-EPMC3910147 | biostudies-literature
Project description:Bacterial gene transfer agents (GTAs) are small virus-like particles that package DNA fragments and inject them into cells. They are encoded by gene clusters resembling defective prophages, with genes for capsid head and tail components. These gene clusters are usually assumed to be maintained by selection for the benefits of GTA-mediated recombination, but this has never been tested. We rigorously examined the potential benefits of GTA-mediated recombination, considering separately transmission of GTA-encoding genes and recombination of all chromosomal genes. In principle GTA genes could be directly maintained if GTA particles spread them to GTA- cells often enough to compensate for the loss of GTA-producing cells. However, careful bookkeeping showed that losses inevitably exceed gains for two reasons. First, cells must lyse to release particles to the environment. Second, GTA genes are not preferentially replicated before DNA is packaged. A simulation model was then used to search for conditions where recombination of chromosomal genes makes GTA+ populations fitter than GTA- populations. Although the model showed that both synergistic epistasis and some modes of regulation could generate fitness benefits large enough to overcome the cost of lysis, these benefits neither allowed GTA+ cells to invade GTA- populations, nor allowed GTA+ populations to resist invasion by GTA- cells. Importantly, the benefits depended on highly improbable assumptions about the efficiencies of GTA production and recombination. Thus, the selective benefits that maintain GTA gene clusters over many millions of years must arise from consequences other than transfer of GTA genes or recombination of chromosomal genes.
| S-EPMC6209664 | biostudies-literature
Project description:BackgroundThe Amoebozoa constitute one of the primary divisions of eukaryotes, encompassing taxa of both biomedical and evolutionary importance, yet its genomic diversity remains largely unsampled. Here we present an analysis of a whole genome assembly of Acanthamoeba castellanii (Ac) the first representative from a solitary free-living amoebozoan.ResultsAc encodes 15,455 compact intron-rich genes, a significant number of which are predicted to have arisen through inter-kingdom lateral gene transfer (LGT). A majority of the LGT candidates have undergone a substantial degree of intronization and Ac appears to have incorporated them into established transcriptional programs. Ac manifests a complex signaling and cell communication repertoire, including a complete tyrosine kinase signaling toolkit and a comparable diversity of predicted extracellular receptors to that found in the facultatively multicellular dictyostelids. An important environmental host of a diverse range of bacteria and viruses, Ac utilizes a diverse repertoire of predicted pattern recognition receptors, many with predicted orthologous functions in the innate immune systems of higher organisms.ConclusionsOur analysis highlights the important role of LGT in the biology of Ac and in the diversification of microbial eukaryotes. The early evolution of a key signaling facility implicated in the evolution of metazoan multicellularity strongly argues for its emergence early in the Unikont lineage. Overall, the availability of an Ac genome should aid in deciphering the biology of the Amoebozoa and facilitate functional genomic studies in this important model organism and environmental host.
| S-EPMC4053784 | biostudies-literature
Project description:Chronic lymphocytic leukemia (CLL) is a very common and mostly incurable B-cell malignancy. Recent studies revealed high interpatient mutational heterogeneity and worsened therapy response and survival of patients with complex genomic aberrations. In line with this, a better understanding of the underlying mechanisms of specific genetic aberrations would reveal new prognostic factors and possible therapeutic targets. It is known that chromosomal rearrangements including DNA insertions often play a role during carcinogenesis. Recently it was reported that bacteria (microbiome)-human lateral gene transfer occurs in somatic cells and is enriched in cancer samples. To further investigate this mechanism in CLL, we analyzed paired-end RNA sequencing data of 45 CLL patients and 9 healthy donors, in which we particularly searched for bacterial DNA integrations into the human somatic genome. Applying the Burrows-Wheeler aligner (BWA) first on a human genome and then on bacterial genome references, we differentiated between sequencing reads mapping to the human genome, to the microbiome or to bacterial integrations into the human genome. Our results indicate that CLL samples featured bacterial DNA integrations more frequently (approx. two-fold) compared to normal samples, which corroborates the latest findings in other cancer entities. Moreover, we determined common integration sites and recurrent integrated bacterial transcripts. Finally, we investigated the contribution of bacterial integrations to oncogenesis and disease progression.
| S-EPMC8835664 | biostudies-literature
Project description:Lateral gene transfer is an important mechanism of natural variation among prokaryotes, but the significance of its quantitative contribution to genome evolution is debated. Here, we report networks that capture both vertical and lateral components of evolutionary history among 539,723 genes distributed across 181 sequenced prokaryotic genomes. Partitioning of these networks by an eigenspectrum analysis identifies community structure in prokaryotic gene-sharing networks, the modules of which do not correspond to a strictly hierarchical prokaryotic classification. Our results indicate that, on average, at least 81 +/- 15% of the genes in each genome studied were involved in lateral gene transfer at some point in their history, even though they can be vertically inherited after acquisition, uncovering a substantial cumulative effect of lateral gene transfer on longer evolutionary time scales.
| S-EPMC2474566 | biostudies-literature
Project description:Bacteria frequently exhibit cooperative behaviors but cooperative strains are vulnerable to invasion by cheater strains that reap the benefits of cooperation but do not perform the cooperative behavior themselves. Bacterial genomes often contain mobile genetic elements such as plasmids. When a gene for cooperative behavior exists on a plasmid, cheaters can be forced to cooperate by infection with this plasmid, rescuing cooperation in a population in which mutation or migration has allowed cheaters to arise. Here we introduce a second plasmid that does not code for cooperation and show that the social dilemma repeats itself at the plasmid level in both within-patch and metapopulation scenarios, and under various scenarios of plasmid incompatibility. Our results suggest that although plasmid carriage of cooperative genes can provide a transient defense against defection in structured environments, plasmid and chromosomal defection remain the only stable strategies in an unstructured environment. We discuss our results in the light of recent bioinformatic evidence that cooperative genes are overrepresented on mobile elements.
| S-EPMC3038327 | biostudies-other
Project description:Mycobacterium tuberculosis is a high GC Gram-positive member of the actinobacteria. The mycobacterial cell wall is composed of a complex assortment of lipids and is the interface between the bacterium and its environment. The biosynthesis of fatty acids plays an essential role in the formation of cell wall components, in particular mycolic acids, which have been targeted by many of the drugs used to treat M. tuberculosis infection. M. tuberculosis has approximately 250 genes involved in fatty acid metabolism, a much higher proportion than in any other organism. In silico methods have been used to compare the genome of M. tuberculosis CDC1551 to a database of 58 complete bacterial genomes. The resulting alignments were scanned for genes specifically involved in fatty acid biosynthetic pathway I. Phylogenetic analysis of these alignments was used to investigate horizontal gene transfer, gene duplication, and adaptive evolution. It was found that of the eight gene families examined, five of the phylogenies reconstructed suggest that the actinobacteria have a closer relationship with the alpha-proteobacteria than expected. This is either due to either an ancient transfer of genes or deep paralogy and subsequent retention of the genes in unrelated lineages. Additionally, adaptive evolution and gene duplication have been an influence in the evolution of the pathway. This study provides a key insight into how M. tuberculosis has developed its unique fatty acid synthetic abilities.
| S-EPMC193559 | biostudies-literature
Project description:BackgroundGenomes of Methanosarcina spp. are among the largest archaeal genomes. One suggested reason for that is massive horizontal gene transfer (HGT) from bacteria. Genes of bacterial origin may be involved in the central metabolism and solute transport, in particular sugar synthesis, sulfur metabolism, phosphate metabolism, DNA repair, transport of small molecules etc. Horizontally transferred (HT) genes are considered to play the key role in the ability of Methanosarcina spp. to inhabit diverse environments. At the moment, genomes of three Methanosarcina spp. have been sequenced, and while these genomes vary in length and number of protein-coding genes, they all have been shown to accumulate HT genes. However, previous estimates had been made when fewer archaeal genomes were known. Moreover, several Methanosarcinaceae genomes from other genera have been sequenced recently. Here, we revise the census of genes of bacterial origin in Methanosarcinaceae.ResultsAbout 5% of Methanosarcina genes have been shown to be horizontally transferred from various bacterial groups to the last common ancestor either of Methanosarcinaceae, or Methanosarcina, or later in the evolution. Simulation of the composition of the NCBI protein non-redundant database for different years demonstrates that the estimates of the HGT rate have decreased drastically since 2002, the year of publication of the first Methanosarcina genome. The phylogenetic distribution of HT gene donors is non-uniform. Most HT genes were transferred from Firmicutes and Proteobacteria, while no HGT events from Actinobacteria to the common ancestor of Methanosarcinaceae were found. About 50% of HT genes are involved in metabolism. Horizontal transfer of transcription factors is not common, while 46% of horizontally transferred genes have demonstrated differential expression in a variety of conditions. HGT of complete operons is relatively infrequent and half of HT genes do not belong to operons.ConclusionsWhile genes of bacterial origin are still more frequent in Methanosarcinaceae than in other Archaea, most HGT events described earlier as Methanosarcina-specific seem to have occurred before the divergence of Methanosarcinaceae. Genes horizontally transferred from bacteria to archaea neither tend to be transferred with their regulators, nor in long operons.
| S-EPMC4455057 | biostudies-literature