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Assessing the benefits of horizontal gene transfer by laboratory evolution and genome sequencing.

ABSTRACT: BACKGROUND:Recombination is widespread across the tree of life, because it helps purge deleterious mutations and creates novel adaptive traits. In prokaryotes, it often takes the form of horizontal gene transfer from a donor to a recipient bacterium. While such transfer is widespread in natural communities, its immediate fitness benefits are usually unknown. We asked whether any such benefits depend on the environment, and on the identity of donor and recipient strains. To this end, we adapted Escherichia coli to two novel carbon sources over several hundred generations of laboratory evolution, exposing evolving populations to various DNA donors. RESULTS:At the end of these experiments, we measured fitness and sequenced the genomes of 65 clones from 34 replicate populations to study the genetic changes associated with adaptive evolution. Furthermore, we identified candidate de novo beneficial mutations. During adaptive evolution on the first carbon source, 4-Hydroxyphenylacetic acid (HPA), recombining populations adapted better, which was likely mediated by acquiring the hpa operon from the donor. In contrast, recombining populations did not adapt better to the second carbon source, butyric acid, even though they suffered fewer extinctions than non-recombining populations. The amount of DNA transferred, but not its benefit, strongly depended on the donor-recipient strain combination. CONCLUSIONS:To our knowledge, our study is the first to investigate the genomic consequences of prokaryotic recombination and horizontal gene transfer during laboratory evolution. It shows that the benefits of recombination strongly depend on the environment and the foreign DNA donor.

SUBMITTER: Chu HY

PROVIDER: S-EPMC5909237 | biostudies-literature | 2018 Apr

REPOSITORIES: biostudies-literature

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Assessing the benefits of horizontal gene transfer by laboratory evolution and genome sequencing.

Chu Hoi Yee HY Sprouffske Kathleen K Wagner Andreas A

BMC evolutionary biology 20180419 1

<h4>Background</h4>Recombination is widespread across the tree of life, because it helps purge deleterious mutations and creates novel adaptive traits. In prokaryotes, it often takes the form of horizontal gene transfer from a donor to a recipient bacterium. While such transfer is widespread in natural communities, its immediate fitness benefits are usually unknown. We asked whether any such benefits depend on the environment, and on the identity of donor and recipient strains. To this end, we a ...[more]

PMID: 29673327

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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.

Project description:Acid mine drainage (AMD), associated with active and abandoned mining sites, is a habitat for acidophilic microorganisms that gain energy from the oxidation of reduced sulfur compounds and ferrous iron and that thrive at pH below 4. Members of the recently proposed genus "Ferrovum" are the first acidophilic iron oxidizers to be described within the Betaproteobacteria. Although they have been detected as typical community members in AMD habitats worldwide, knowledge of their phylogenetic and metabolic diversity is scarce. Genomics approaches appear to be most promising in addressing this lacuna since isolation and cultivation of "Ferrovum" has proven to be extremely difficult and has so far only been successful for the designated type strain "Ferrovum myxofaciens" P3G. In this study, the genomes of two novel strains of "Ferrovum" (PN-J185 and Z-31) derived from water samples of a mine water treatment plant were sequenced. These genomes were compared with those of "Ferrovum" sp. JA12 that also originated from the mine water treatment plant, and of the type strain (P3G). Phylogenomic scrutiny suggests that the four strains represent three "Ferrovum" species that cluster in two groups (1 and 2). Comprehensive analysis of their predicted metabolic pathways revealed that these groups harbor characteristic metabolic profiles, notably with respect to motility, chemotaxis, nitrogen metabolism, biofilm formation and their potential strategies to cope with the acidic environment. For example, while the "F. myxofaciens" strains (group 1) appear to be motile and diazotrophic, the non-motile group 2 strains have the predicted potential to use a greater variety of fixed nitrogen sources. Furthermore, analysis of their genome synteny provides first insights into their genome evolution, suggesting that horizontal gene transfer and genome reduction in the group 2 strains by loss of genes encoding complete metabolic pathways or physiological features contributed to the observed diversification.

Project description:Horizontal gene transfer (HGT) is the process through which genetic information is transferred between different genomes and that played a crucial role in bacterial evolution. HGT can enable bacteria to rapidly acquire antibiotic resistance and bacteria that have acquired resistance is spreading within the microbiome. Conventional methods of characterizing HGT patterns include short-read metagenomic sequencing (short-reads mNGS), long-read sequencing, and single-cell sequencing. These approaches present several limitations, such as short-read fragments, high amounts of input DNA, and sequencing costs, respectively. Here, we attempt to circumvent present limitations to detect HGT by developing a metagenomics co-barcode sequencing workflow (MECOS) and applying it to the human and mouse gut microbiomes. In addition to that, we have over 10-fold increased contig length compared to short-reads mNGS; we also obtained exceeding 30 million paired reads with co-barcode information. Applying the novel bioinformatic pipeline, we integrated this co-barcoding information and the context information from long reads, and observed over 50-fold HGT events after we corrected the potential wrong HGT events. Specifically, we detected approximately 3,000 HGT blocks in individual samples, encompassing ~6,000 genes and ~100 taxonomic groups, including loci conferring tetracycline resistance through ribosomal protection. MECOS provides a valuable tool for investigating HGT and advance our understanding on the evolution of natural microbial communities within hosts.IMPORTANCEIn this study, to better identify horizontal gene transfer (HGT) in individual samples, we introduce a new co-barcoding sequencing system called metagenomics co-barcoding sequencing (MECOS), which has three significant improvements: (i) long DNA fragment extraction, (ii) a special transposome insertion, (iii) hybridization of DNA to barcode beads, and (4) an integrated bioinformatic pipeline. Using our approach, we have over 10-fold increased contig length compared to short-reads mNGS, and observed over 50-fold HGT events after we corrected the potential wrong HGT events. Our results indicate the presence of approximately 3,000 HGT blocks, involving roughly 6,000 genes and 100 taxonomic groups in individual samples. Notably, these HGT events are predominantly enriched in genes that confer tetracycline resistance via ribosomal protection. MECOS is a useful tool for investigating HGT and the evolution of natural microbial communities within hosts, thereby advancing our understanding of microbial ecology and evolution.

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Assessing the benefits of horizontal gene transfer by laboratory evolution and genome sequencing.

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Assessing the benefits of horizontal gene transfer by laboratory evolution and genome sequencing.

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