Highways of gene sharing in prokaryotes

Abstract

The extent to which lateral genetic transfer has shaped microbial genomes has major implications for the emergence of community structures. We have performed a rigorous phylogenetic analysis of >220,000 proteins from genomes of 144 prokaryotes to determine the contribution of gene sharing to current prokaryotic diversity, and to identify ''highways'' of sharing between lineages. The inferred relationships suggest a pattern of inheritance that is largely vertical, but with notable exceptions among closely related taxa, and among distantly related organisms that live in similar environments.lateral genetic transfer ͉ microbial genomes ͉ molecular phylogeny B eginning in the 1980s, recognition of the 16S ribosomal RNA gene (rDNA) as a molecular chronometer (1), the development of automated sequencing technology and PCR, and improved phylogenetic methods (2) converged to yield a universal phylogenetic tree (1, 3) that was often interpreted as the ''tree of life.'' However, trees inferred from protein-coding genes or proteins are not always topologically congruent with the rDNA tree (4, 5) or with one another (6, 7). Instances of incongruence are often attributed to historical transfers of genetic information from one genealogical lineage to another (8). Mechanisms for lateral genetic transfer (LGT) are well characterized, and in a laboratory context underpin much of the biotechnology industry. At issue, however, is the extent to which LGT has contributed to the natural diversity of prokaryotes. If LGT has been rampant and consequential, there may in fact be no universal tree of life, and attempts to construct a phylogenetic classification of prokaryotes based on molecular sequence information will ultimately be futile (9).Least controversial among proposed LGT events are transfers that span relatively short evolutionary distances, where the donor and recipient organisms are members of the same species. DNA exchanges between close relatives are likely to be successful because of compatible methods of genetic exchange such as conjugation and the increased likelihood of homologous recombination between the donated DNA and the recipient genome (10). Linkage disequilibrium analysis of environmental samples has revealed extensive homologous recombination within many species of prokaryotes (11). Transfers between distantly related taxa are much less likely to succeed, because conjugation or viral transduction of genes between different species is less common (although not impossible), and foreign DNA must be integrated into the genome via illegitimate rather than homologous recombination (10). However, if organisms in the environment are subjected to a constant ''rain'' of DNA (12), then these rare processes will occur in evolutionary time, and will be fixed in a lineage especially if they confer a selective advantage on the recipient organism.LGT has tremendous implications for the genesis and evolution of microbial communities: if extensive LGT can occur among distantly related organisms, then processes such as niche inv...

Inter-phylum HGT has shaped the metabolism of many mesophilic and anaerobic bacteria

“…Extensive HGT among thermophiles, pathogens and cyanobacteria has been described previously, for example, 'highways' of HGT (Doolittle, 1998;Beiko et al, 2005), and was attributed to substantial ecological overlap among the partners involved. Along the same lines, a recent study of intra-phylum HGT showed that very recent gene transfer events (reflected by 499% nucleotide sequence identity) are clearly structured by ecology, where the highest frequency of HGT was observed among organisms recovered from the same site of the human body (Smillie et al, 2011).…”

“…In fact, recent analysis of protein families suggests that HGT, and not gene duplication, has driven protein expansion and functional novelty in bacteria, which is in contrast with most eukaryotic organisms (Treangen and Rocha, 2011). Sequencing of thousands of microbial genomes during the past two decades has allowed the identification of HGT events at different timescales, from ancestral to recent events, and between organisms of varied evolutionary relatedness, from closely related genomes to very distantly related ones (Gogarten et al, 2002;Beiko et al, 2005;Ochman et al, 2005;Zhaxybayeva et al, 2009a), revealing that HGT has affected the evolutionary history of most, if not all, bacterial lineages.…”

Gene transfer agents: phage-like elements of genetic exchange

“…6,9,11,12 . Such patterns are probably a consequence of existing barriers to HGT, which have been reviewed in detail elsewhere 13,14 .…”

Dealing with incongruence in phylogenomic analyses

“…An extreme case is genome chimerism, as discussed previously. As far as bacteria are concerned, neither Beiko et al (2005) nor Ge et al (2005) detected strong evidence for preferential genetic exchanges between specific phyla: according to these studies, bacterial gene trees are more or less randomly distributed around the species tree (but see Matte-Taillez et al 2002;Jain et al 2003). We note that there is a convergence between practical and conceptual aspects here; the task of reconstructing 'the' species tree is more and more difficult, and more and more pointless, as the distribution of true gene trees becomes multimodal.…”