The role of lateral gene transfer in the evolution of isoprenoid biosynthesis pathways

Abstract

SummaryLateral gene transfer (LGT) is a major force in microbial genome evolution. Here, we present an overview of lateral transfers affecting genes involved in isopentenyl diphosphate (IPP) synthesis. Two alternative metabolic pathways can synthesize this universal precursor of isoprenoids, the 1-deoxy-Dxylulose 5-phosphate (DOXP) pathway and the mevalonate (MVA) pathway. We have surveyed recent genomic data and the biochemical literature to determine the distribution of the genes composing these pathways within the bacterial domain. The scattered distribution observed is incompatible with a simple scheme of vertical transmission.LGT (among and between bacteria, archaea and eukaryotes) more parsimoniously explains many features of this pattern. This alternative scenario is supported by phylogenetic analyses, which unambiguously confirm several cases of lateral transfer. Available biochemical data allow the formulation of hypotheses about selective pressures favouring transfer. The phylogenetic diversity of the organisms involved and the range of possible causes and effects of these transfer events make the IPP biosynthetic pathways an ideal system for studying the evolutionary role of LGT.

The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification.

“…In particular, there is no evidence whatever that the two pathways evolved in different groups. Boucher & Doolittle (2000) do, however, present evidence for homologous gene replacement within the mevalonate pathway itself for HMG-CoA reductase, which makes the mevalonate. All HMG-CoA reductases are related, but form two sharply distinct clusters on trees.…”

“…All neomuran enzymes are class 1, except those of the eukaryote Giardia and the archaebacterium Archaeoglobus, which are class 2 enzymes. In the present state of knowledge, the suggestion that these two sequences were acquired by lateral gene transfer from eubacteria (Boucher & Doolittle, 2000) is rather convincing. But I do not agree with their conclusion that lateral gene transfer also occurred between eubacteria.…”

“…Consider the case of the evolution of isoprenoid biosynthesis in bacteria, recently well reviewed from a lateral gene transfer perspective (Boucher & Doolittle, 2000). Two different non-homologous multienzyme pathways are very widespread in bacteria.…”

“…I predict that, when careful studies are done, gene losses will be found to be at least two orders of magnitude more common than lateral gene transfer in eukaryotes (excluding the very rare special case of cellular symbiogenesis that can simultaneously implant thousands of genes) and probably an order of magnitude more common in bacteria. If lateral transfer took hold as a null hypothesis or dogma, rather than as one of several possible explanations for conflicting trees, studies to test this would be impeded.Consider the case of the evolution of isoprenoid biosynthesis in bacteria, recently well reviewed from a lateral gene transfer perspective (Boucher & Doolittle, 2000). Two different non-homologous multienzyme pathways are very widespread in bacteria.…”

Design, Synthesis, and X-ray Crystallographic Studies of α-Aryl Substituted Fosmidomycin Analogues as Inhibitors of Mycobacterium tuberculosis 1-Deoxy-d-xylulose 5-Phosphate Reductoisomerase

“…In other eukaryotes as well as archaea, 5 IPP is instead formed through the classical mevalonate pathway, 6 starting from acetyl-CoA. The different routes used for IPP synthesis suggest that all enzymes within the non-mevalonate pathway are potentially interesting targets for new drugs against many pathogens, including M. tuberculosis.…”