Origin and Evolution of Polycyclic Triterpene Synthesis

Mol Biol Evol. 2020 Jul 1;37(7):1925-1941. doi: 10.1093/molbev/msaa054.

Abstract

Polycyclic triterpenes are members of the terpene family produced by the cyclization of squalene. The most representative polycyclic triterpenes are hopanoids and sterols, the former are mostly found in bacteria, whereas the latter are largely limited to eukaryotes, albeit with a growing number of bacterial exceptions. Given their important role and omnipresence in most eukaryotes, contrasting with their scant representation in bacteria, sterol biosynthesis was long thought to be a eukaryotic innovation. Thus, their presence in some bacteria was deemed to be the result of lateral gene transfer from eukaryotes. Elucidating the origin and evolution of the polycyclic triterpene synthetic pathways is important to understand the role of these compounds in eukaryogenesis and their geobiological value as biomarkers in fossil records. Here, we have revisited the phylogenies of the main enzymes involved in triterpene synthesis, performing gene neighborhood analysis and phylogenetic profiling. Squalene can be biosynthesized by two different pathways containing the HpnCDE or Sqs proteins. Our results suggest that the HpnCDE enzymes are derived from carotenoid biosynthesis ones and that they assembled in an ancestral squalene pathway in bacteria, while remaining metabolically versatile. Conversely, the Sqs enzyme is prone to be involved in lateral gene transfer, and its emergence is possibly related to the specialization of squalene biosynthesis. The biosynthesis of hopanoids seems to be ancestral in the Bacteria domain. Moreover, no triterpene cyclases are found in Archaea, invoking a potential scenario in which eukaryotic genes for sterol biosynthesis assembled from ancestral bacterial contributions in early eukaryotic lineages.

Keywords: carotenoids; eukaryogenesis; lateral gene transfer; polycyclic triterpenes; squalene.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Carotenoids / metabolism*
  • Eukaryota / metabolism
  • Evolution, Molecular*
  • Farnesyl-Diphosphate Farnesyltransferase / genetics*
  • Farnesyl-Diphosphate Farnesyltransferase / metabolism
  • Genes, Bacterial
  • Phylogeny*
  • Squalene / metabolism*
  • Sterols / biosynthesis

Substances

  • Sterols
  • Carotenoids
  • Squalene
  • Farnesyl-Diphosphate Farnesyltransferase