Integration of a Foreign Gene into a Native Complex Does Not Impair Fitness in an Experimental Model of Lateral Gene Transfer

Lateral gene transfer (LGT) is a central force in microbial evolution. The observation that genes encoding subunits of complexes exhibit relatively compatible phylogenies, suggesting vertical descent, can be explained by different evolutionary scenarios. On the one hand, the failure of a new gene product to correctly interact with preexisting protein subunits can make its acquisition neutral-a theory termed the "complexity hypothesis." On the other hand, foreign subunit-encoding genes may reduce the fitness of the new host by disrupting the stoichiometric balance between complex subunits, resulting in purifying selection against gene retention. We previously showed in a model LGT system that overexpression of an orthologous subunit was neutral due to lack of interaction with host subunits. Here, we examine a case where the foreign protein is more similar to its native orthologs, by expressing the RNA polymerase beta subunit (RpoB) of Bacillus subtilis in Escherichia coli. The foreign subunit is shown by coimmunoprecipitation to interact with the host subunits, and to form novel, nonspecific interactions. Nevertheless, the host did not incur any fitness disadvantage, as measured by its growth. We conclude that LGT of complex subunits may be neutral even when the transferred subunit can integrate into the host complex and that this neutrality can be a fertile ground for selective forces once the environment changes.