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Prediction of Horizontally and Widely Transferred Genes in Prokaryotes.

ABSTRACT: Horizontal gene transfer (HGT) is the process whereby an organism acquires exogenous genes (horizontally transferred genes or HT genes) that are not inherited from the parent, but are derived from another organism. In prokaryotes, HGT has been considered as one of the important driving forces of evolution. Previously, genome-wide analyses have been conducted for estimating the proportion of HT genes in prokaryotic genomes, but the number of species examined at the time was limited, and gene annotation was relatively poor. Currently, tens of thousands of prokaryotic genomes have been published and gene annotation resources have improved. In the present study, HT gene prediction method was modified so that the estimate was robust to gene length, conducting a comprehensive search using 3017 representative prokaryotic genomes belonging to 1348 species. The result showed that an average of 13% (ranging from 0% to 30% across species) of protein-coding genes was predicted as being of horizontal origin. The proportion of the predicted HT genes per species was associated with the species' habitat, while a positive correlation between the proportion and genomic nucleotide frequency was also observed. Moreover, the functions of the predicted HT genes were inferred and compared according to two popular databases, the Clusters of Orthologous Groups and the Kyoto Encyclopedia of Genes and Genomes. As a result, both databases indicated that many of the widely transferred genes were involved in mobile genetic elements (transposons, phages, and plasmids) as expected. Notably, the present study predicted that six as-yet-uncharacterized genes were widely distributed HT genes, and therefore, will be interesting targets for evolutionary studies. Thus, this study demonstrates that a data-driven approach using massive sequence data may contribute to a broader understanding of HGT in prokaryotes.

SUBMITTER: Nakamura Y

PROVIDER: S-EPMC6287321 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Prediction of Horizontally and Widely Transferred Genes in Prokaryotes.

Nakamura Yoji Y

Evolutionary bioinformatics online 20181130

Horizontal gene transfer (HGT) is the process whereby an organism acquires exogenous genes (horizontally transferred genes or HT genes) that are not inherited from the parent, but are derived from another organism. In prokaryotes, HGT has been considered as one of the important driving forces of evolution. Previously, genome-wide analyses have been conducted for estimating the proportion of HT genes in prokaryotic genomes, but the number of species examined at the time was limited, and gene anno ...[more]

PMID: 30546254

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Project description:BackgroundHorizontal gene transfer plays an important role in evolution because it sometimes allows recipient lineages to adapt to new ecological niches. High genes transfer frequencies were inferred for prokaryotic and early eukaryotic evolution. Does horizontal gene transfer also impact phylogenetic reconstruction of the evolutionary history of genomes and organisms? The answer to this question depends at least in part on the actual gene transfer frequencies and on the ability to weed out transferred genes from further analyses. Are the detected transfers mainly false positives, or are they the tip of an iceberg of many transfer events most of which go undetected by current methods?ResultsPhylogenetic detection methods appear to be the method of choice to infer gene transfers, especially for ancient transfers and those followed by orthologous replacement. Here we explore how well some of these methods perform using in silico transfers between the terminal branches of a gamma proteobacterial, genome based phylogeny. For the experiments performed here on average the AU test at a 5% significance level detects 90.3% of the transfers and 91% of the exchanges as significant. Using the Robinson-Foulds distance only 57.7% of the exchanges and 60% of the donations were identified as significant. Analyses using bipartition spectra appeared most successful in our test case. The power of detection was on average 97% using a 70% cut-off and 94.2% with 90% cut-off for identifying conflicting bipartitions, while the rate of false positives was below 4.2% and 2.1% for the two cut-offs, respectively. For all methods the detection rates improved when more intervening branches separated donor and recipient.ConclusionRates of detected transfers should not be mistaken for the actual transfer rates; most analyses of gene transfers remain anecdotal. The method and significance level to identify potential gene transfer events represent a trade-off between the frequency of erroneous identification (false positives) and the power to detect actual transfer events.

Project description:BackgroundHorizontal gene transfer (HGT), a source of genetic variation, is generally considered to facilitate hosts' adaptability to environments. However, convincing evidence supporting the significant contribution of the transferred genes to the evolution of metazoan recipients is rare.ResultsIn this study, based on sequence data accumulated to date, we used a unified method consisting of similarity search and phylogenetic analysis to detect horizontally transferred genes (HTGs) between prokaryotes and five insect species including Drosophila melanogaster, Anopheles gambiae, Bombyx mori, Tribolium castaneum and Apis mellifera. Unexpectedly, the candidate HTGs were not detected in D. melanogaster, An. gambiae and T. castaneum, and 79 genes in Ap. mellifera sieved by the same method were considered as contamination based on other information. Consequently, 14 types of 22 HTGs were detected only in the silkworm. Additionally, 13 types of the detected silkworm HTGs share homologous sequences in species of other Lepidopteran superfamilies, suggesting that the majority of these HTGs were derived from ancient transfer events before the radiation of Ditrysia clade. On the basis of phylogenetic topologies and BLAST search results, donor bacteria of these genes were inferred, respectively. At least half of the predicted donor organisms may be entomopathogenic bacteria. The predicted biochemical functions of these genes include four categories: glycosyl hydrolase family, oxidoreductase family, amino acid metabolism, and others.ConclusionsThe products of HTGs detected in this study may take part in comprehensive physiological metabolism. These genes potentially contributed to functional innovation and adaptability of Lepidopteran hosts in their ancient lineages associated with the diversification of angiosperms. Importantly, our results imply that pathogens may be advantageous to the subsistence and prosperity of hosts through effective HGT events at a large evolutionary scale.

Dataset Information

Prediction of Horizontally and Widely Transferred Genes in Prokaryotes.

Publications

Prediction of Horizontally and Widely Transferred Genes in Prokaryotes.

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