Lateral gene transfer: when will adolescence end?

Abstract

SummaryThe scope and impact of horizontal gene transfer (HGT) in Bacteria and Archaea has grown from a topic largely ignored by the microbiological community to a hot-button issue gaining staunch supporters (on particular points of view) at a seemingly ever-increasing rate. Opinions range from HGT being a phenomenon with minor impact on overall microbial evolution and diversification to HGT being so rampant as to obfuscate any opportunities for elucidating microbial evolution -especially organismal phylogeny -from sequence comparisons. This contentious issue has been fuelled by the influx of complete genome sequences, which has allowed for a more detailed examination of this question than previously afforded. We propose that the lack of common ground upon which to formulate consensus viewpoints probably stems from the absence of answers to four critical questions. If addressed, they could clarify concepts, reject tenuous speculation and solidify a robust foundation for the integration of HGT into a framework for long-term microbial evolution, regardless of the intellectual camp in which you reside. Here, we examine these issues, why their answers shape the outcome of this debate and the progress being made to address them. Coming of ageThe first complete genome sequence of a free-living organism ( Haemophilus influenzae ) was released in 1995 (Fleischmann et al ., 1995) and, as of writing, more than 100 microbial genome sequences representing diverse lineages of Bacteria and Archaea have subsequently become available. The promise for new information held in complete genome sequences is vast and manifold, including (i) insight into previously unsuspected metabolic functions; (ii) elucidation of a microbe's underlying physiology even in the absence of a tractable genetic system or the ability to propagate the organism in pure culture; (iii) the identification of potential drug targets in pathogenic organisms; (iv) observations into the conservation of gene order, operon structure, variation in rates of evolution within and among genes, and so forth. The possibilities for mining novel answers to unasked questions also appear to be nearly endless, and the so-called 'postgenomic era' has indeed brought about the publication of clever investigations that have called attention to hitherto unimagined aspects of microbiology.

Conjugative plasmids: vessels of the communal gene pool

“…These two factors, compactness and gene clustering, mean that many conferrable traits can be transferred between discrete replicating elements (chromosomes or plasmids) by the movement of relatively small fragments of DNA. Phylogenetic analyses of complete genomes have also shown that some prokaryotic genes are more likely to be transferred than others (Lawrence & Hendrickson 2003), which, by deduction, would also reflect their propensity to enter the communal pool. Genes involved in transcription, translation and related processes (informational genes) are less likely to have been successfully transferred horizontally than genes involved in amino acid biosynthesis and other housekeeping functions (operational genes), because they are usually members of large molecular complexes, thus 'the complexity hypothesis' (Rivera et al 1998;Jain et al 1999).…”

“…Gene transfer by means of MGEs is first of all limited by restrictions in the host ranges of elements such as viruses and plasmids. Furthermore, various molecular mechanisms counteract uptake and stabilization of foreign DNA molecules as the phylogenetic distances increase (Lawrence & Hendrickson 2003;Thomas & Nielsen 2005). Nonetheless, an intimate relationship critical to the ecology of the hosts seems to have developed between private and communal pools repeatedly.…”

Early Microbial Evolution: The Age of Anaerobes

“…The issue of how tree-like prokaryote evolution is or is not (because of LGT) is still simmering. Some say that prokaryote evolution is tree-like (Ciccarelli et al 2006;Boussau and Gouy 2012), some say that it is somewhat tree-like (Puigbò et al 2009), some say that "only 1%" is tree-like (Dagan and Martin 2006), some say that we cannot tell, so we should assume that it is tree-like (Forterre 2015), while some say "can we just get on with it" (Lawrence and Hendrickson 2003).…”

The genome of the protist parasite Entamoeba histolytica

“…LGT is an important force in the evolution of prokaryotes but significantly less is known about its importance in eukaryotic evolution 11 . We conducted a phylogenetic screen of the Entamoeba genome for cases of relatively recent prokaryote to eukaryote LGT (see Methods), and for 96 genes we believe that this is the simplest explanation for the tree topologies obtained (see Supplementary Information).…”