Barriers to Horizontal Gene Transfer: Fuzzy and Evolvable Boundaries

The existence of numerous types of barriers to horizontal gene transfer (HGT) is well documented. Nevertheless, no barrier is impervious, and all kinds of genes can occasionally find their way into organisms different from the ones in which they evolved. This by no means implies a free flow of genes across taxa, but, rather, the existence of complex networks of loopholes across barriers that could potentially connect all kinds of organisms through gene transfer. Loopholes may be provided by way of a small fraction of the individuals in an otherwise inaccessible population and, if exogenous genes are incorporated into the chromosome, homology-assisted recombination processes may further spread them across wild type individuals. HGT networks should be very fluid, as they depend heavily on fortuitous events and transient circumstances, such as the presence of mobile genetic elements (MGEs) in a potential donor that may extend the transfer network in particular directions. Moreover, HGT networks should be highly evolvable, as a result of (1) the multiplicity of processes with the potential to modulate, modify or alleviate the different barriers to transfer, (2) the constantly changing selective pressures operating on them and (3) the enormous plasticity of MGEs. Finally, HGT networks should be genespecific, as different genes should have an unequal likelihood of passing through or being incorporated into new genomes. Introduction The controversy surrounding HGT is often polarized into views that attempt to summarize the overall impact of this phenomenon on prokaryotic evolution, particularly regarding the existence of prokaryotic species and of organismal phylogenies (Bapteste and Boucher, 2009; Doolittle and Zhaxybayeva, 2009; Puigbo et al., 2009; Riley and Lizotte-Waniewski, 2009). HGT, however, encompasses a multiplicity of processes, which operate through different agents and mechanisms, rely on different ecological circumstances and result in a wide range of fitness effects on the recipient organisms. In this chapter, we wish to explore the barriers that limit HGT among organisms and the circumstances and manners in which they may be circumvented, following the rationale that taking into account the conditions in which HGT operates should contribute to the development of more specific lines of research on the detailed dynamics of HGT processes and their repercussions on the evolution of prokaryotes.