MBE Advance Access first published online on June 12, 2008
This version published online on June 12, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn131
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Research Article |
Neutrality of foreign complex subunits in an experimental model of lateral gene transfer
Department of Molecular Microbiology and Biotechnology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel, 69978
* Correspondence: Uri Gophna. E-mail: urigo{at}post.tau.ac.il; Tel 972-3-6409988; Fax 972-3-6409407
Received for publication April 2, 2008. Revision received May 25, 2008. Accepted for publication May 25, 2008.
Lateral gene transfer is a powerful force in microbial evolution. However, the barriers that restrict this evolutionary phenomenon are not fully understood. It has long been observed that genes that encode subunits of complexes exhibit relatively compatible phylogenies, implying mostly vertical evolution. This may be explained by the failure of a new gene product to effectively interact with pre-existing protein subunits, making its acquisition neutral – a theory termed the "complexity hypothesis". On the other hand, such genes may reduce the fitness of the host by disturbing the stoichiometric balance between complex subunits, resulting in purifying selection against gene retention. To examine these two alternative scenarios we designed an experimental system that mimics the transfer of genes encoding homologs of essential complex subunits into the model bacterium Escherichia coli. In addition, we over-expressed the native E. coli gene in order to examine the contribution of gene dosage effects. We show that accumulation of native or foreign complex subunits in the cell does not result in loss of fitness, except for a minor fitness reduction observed for a single foreign homolog. Indeed, a series of genetic and biochemical assays failed to detect any interaction between the foreign subunits and the native polypeptides of the complex, implying an inability of such transfer events to generate positive selection for gene retention. We conclude that lateral gene transfer of complex subunits may be mostly neutral and that forces operating against gene retention appear to be moderate.
Key Words: Horizontal gene transfer • complexity hypothesis • balance hypothesis • protein complexes • essential genes • Escherichia coli