Complexity, connectivity, and duplicability as barriers to lateral gene transfer

BACKGROUND: Lateral gene transfer is a major force in microbial evolution and a great source of genetic innovation in prokaryotes. Protein complexity has been claimed to be a barrier for gene transfer, due to either the inability of a new gene's encoded protein to become a subunit of an existin...

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Autores principales: Wellner, Alon, Lurie, Mor N, Gophna, Uri
Formato: Texto
Lenguaje:English
Publicado: BioMed Central 2007
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2374987/
https://www.ncbi.nlm.nih.gov/pubmed/17678544
http://dx.doi.org/10.1186/gb-2007-8-8-r156
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author Wellner, Alon
Lurie, Mor N
Gophna, Uri
author_facet Wellner, Alon
Lurie, Mor N
Gophna, Uri
author_sort Wellner, Alon
collection PubMed
description BACKGROUND: Lateral gene transfer is a major force in microbial evolution and a great source of genetic innovation in prokaryotes. Protein complexity has been claimed to be a barrier for gene transfer, due to either the inability of a new gene's encoded protein to become a subunit of an existing complex (lack of positive selection), or from a harmful effect exerted by the newcomer on native protein assemblages (negative selection). RESULTS: We tested these scenarios using data from the model prokaryote Escherichia coli. Surprisingly, the data did not support an inverse link between membership in protein complexes and gene transfer. As the complexity hypothesis, in its strictest sense, seemed valid only to essential complexes, we broadened its scope to include connectivity in general. Transferred genes are found to be less involved in protein-protein interactions, outside stable complexes, and this is especially true for genes recently transferred to the E. coli genome. Thus, subsequent to transfer, new genes probably integrate slowly into existing protein-interaction networks. We show that a low duplicability of a gene is linked to a lower chance of being horizontally transferred. Notably, many essential genes in E. coli are conserved as singletons across multiple related genomes, have high connectivity and a highly vertical phylogenetic signal. CONCLUSION: High complexity and connectivity generally do not impede gene transfer. However, essential genes that exhibit low duplicability and high connectivity do exhibit mostly vertical descent.
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spelling pubmed-23749872008-05-10 Complexity, connectivity, and duplicability as barriers to lateral gene transfer Wellner, Alon Lurie, Mor N Gophna, Uri Genome Biol Research BACKGROUND: Lateral gene transfer is a major force in microbial evolution and a great source of genetic innovation in prokaryotes. Protein complexity has been claimed to be a barrier for gene transfer, due to either the inability of a new gene's encoded protein to become a subunit of an existing complex (lack of positive selection), or from a harmful effect exerted by the newcomer on native protein assemblages (negative selection). RESULTS: We tested these scenarios using data from the model prokaryote Escherichia coli. Surprisingly, the data did not support an inverse link between membership in protein complexes and gene transfer. As the complexity hypothesis, in its strictest sense, seemed valid only to essential complexes, we broadened its scope to include connectivity in general. Transferred genes are found to be less involved in protein-protein interactions, outside stable complexes, and this is especially true for genes recently transferred to the E. coli genome. Thus, subsequent to transfer, new genes probably integrate slowly into existing protein-interaction networks. We show that a low duplicability of a gene is linked to a lower chance of being horizontally transferred. Notably, many essential genes in E. coli are conserved as singletons across multiple related genomes, have high connectivity and a highly vertical phylogenetic signal. CONCLUSION: High complexity and connectivity generally do not impede gene transfer. However, essential genes that exhibit low duplicability and high connectivity do exhibit mostly vertical descent. BioMed Central 2007 2007-08-02 /pmc/articles/PMC2374987/ /pubmed/17678544 http://dx.doi.org/10.1186/gb-2007-8-8-r156 Text en Copyright © 2007 Wellner et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an open access article distributed under the terms of the Creative Commons Attribution License ( (http://creativecommons.org/licenses/by/2.0) ), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research
Wellner, Alon
Lurie, Mor N
Gophna, Uri
Complexity, connectivity, and duplicability as barriers to lateral gene transfer
title Complexity, connectivity, and duplicability as barriers to lateral gene transfer
title_full Complexity, connectivity, and duplicability as barriers to lateral gene transfer
title_fullStr Complexity, connectivity, and duplicability as barriers to lateral gene transfer
title_full_unstemmed Complexity, connectivity, and duplicability as barriers to lateral gene transfer
title_short Complexity, connectivity, and duplicability as barriers to lateral gene transfer
title_sort complexity, connectivity, and duplicability as barriers to lateral gene transfer
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2374987/
https://www.ncbi.nlm.nih.gov/pubmed/17678544
http://dx.doi.org/10.1186/gb-2007-8-8-r156
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