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

ABSTRACT: 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. RESULTS: We classified the E. coli genes into three categories based on their evolutionary conservation: a set of 2158 Core genes that are shared by all E. coli strains, a set of 1044 Non-core genes that are strain-specific, and a set of 1053 genes that were putatively acquired by horizontal transfer. We observed a clear correlation between gene expressivity (measured by Codon Adaptation Index), evolutionary rates, and node connectivity between these categories of genes. Specifically, we found the Core genes are the most highly expressed and the most slowly evolving, while the HGT genes are expressed at the lowest level and evolve at the highest rate. Core genes are the most likely and HGT genes are the least likely to be member of the operons. In addition, we found the Core genes on average are more highly connected than Non-core and HGT genes in the protein interaction network, however the HGT genes displayed a significantly higher mean node degree than the Core and Non-core genes in the defence COG functional category. Interestingly, HGT genes are more likely to be connected to Core genes than expected by chance, which suggest a model of differential attachment in the expansion of cellular networks. CONCLUSION: Results from our analysis shed light on the mode and mechanism of the integration of horizontally transferred genes into operons and protein interaction networks.

SUBMITTER: Davids W

PROVIDER: S-EPMC2259305 | biostudies-literature | 2008

REPOSITORIES: biostudies-literature

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

Davids Wagied W Zhang Zhaolei Z

BMC evolutionary biology 20080124

<h4>Background</h4>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.<h4>Results</h4>We classified the E. coli genes into three categories based on their evolutionary conservation: a set of ...[more]

PMID: 18218112

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Project description:BackgroundMany biological networks show some characteristics of scale-free networks. Scale-free networks can evolve through preferential attachment where new nodes are preferentially attached to well connected nodes. In networks which have evolved through preferential attachment older nodes should have a higher average connectivity than younger nodes. Here we have investigated preferential attachment in the context of metabolic networks.ResultsThe connectivities of the enzymes in the metabolic network of Escherichia coli were determined and representatives for these enzymes were located in 11 eukaryotes, 17 archaea and 46 bacteria. E. coli enzymes which have representatives in eukaryotes have a higher average connectivity while enzymes which are represented only in the prokaryotes, and especially the enzymes only present in betagamma-proteobacteria, have lower connectivities than expected by chance. Interestingly, the enzymes which have been proposed as candidates for horizontal gene transfer have a higher average connectivity than the other enzymes. Furthermore, It was found that new edges are added to the highly connected enzymes at a faster rate than to enzymes with low connectivities which is consistent with preferential attachment.ConclusionHere, we have found indications of preferential attachment in the metabolic network of E. coli. A possible biological explanation for preferential attachment growth of metabolic networks is that novel enzymes created through gene duplication maintain some of the compounds involved in the original reaction, throughout its future evolution. In addition, we found that enzymes which are candidates for horizontal gene transfer have a higher average connectivity than other enzymes. This indicates that while new enzymes are attached preferentially to highly connected enzymes, these highly connected enzymes have sometimes been introduced into the E. coli genome by horizontal gene transfer. We speculate that E. coli has adjusted its metabolic network to a changing environment by replacing the relatively central enzymes for better adapted orthologs from other prokaryotic species.

Project description:BackgroundShuffling and disruption of operons and horizontal gene transfer are major contributions to the new, dynamic view of prokaryotic evolution. Under the 'selfish operon' hypothesis, operons are viewed as mobile genetic entities that are constantly disseminated via horizontal gene transfer, although their retention could be favored by the advantage of coregulation of functionally linked genes. Here we apply comparative genomics and phylogenetic analysis to examine horizontal transfer of entire operons versus displacement of individual genes within operons by horizontally acquired orthologs and independent assembly of the same or similar operons from genes with different phylogenetic affinities.ResultsSince a substantial number of operons have been identified experimentally in only a few model bacteria, evolutionarily conserved gene strings were analyzed as surrogates of operons. The phylogenetic affinities within these predicted operons were assessed first by sequence similarity analysis and then by phylogenetic analysis, including statistical tests of tree topology. Numerous cases of apparent horizontal transfer of entire operons were detected. However, it was shown that apparent horizontal transfer of individual genes or arrays of genes within operons is not uncommon either and results in xenologous gene displacement in situ, that is, displacement of an ancestral gene by a horizontally transferred ortholog from a taxonomically distant organism without change of the local gene organization. On rarer occasions, operons might have evolved via independent assembly, in part from horizontally acquired genes.ConclusionsThe discovery of in situ gene displacement shows that combination of rampant horizontal gene transfer with selection for preservation of operon structure provides for events in prokaryotic evolution that, a priori, seem improbable. These findings also emphasize that not all aspects of operon evolution are selfish, with operon integrity maintained by purifying selection at the organism level.

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

Publications

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

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