Terpene synthase genes in eukaryotes beyond plants and fungi: Occurrence in social amoebae

Proc Natl Acad Sci U S A. 2016 Oct 25;113(43):12132-12137. doi: 10.1073/pnas.1610379113. Epub 2016 Oct 7.

Abstract

Terpenes are structurally diverse natural products involved in many ecological interactions. The pivotal enzymes for terpene biosynthesis, terpene synthases (TPSs), had been described only in plants and fungi in the eukaryotic domain. In this report, we systematically analyzed the genome sequences of a broad range of nonplant/nonfungus eukaryotes and identified putative TPS genes in six species of amoebae, five of which are multicellular social amoebae from the order of Dictyosteliida. A phylogenetic analysis revealed that amoebal TPSs are evolutionarily more closely related to fungal TPSs than to bacterial TPSs. The social amoeba Dictyostelium discoideum was selected for functional study of the identified TPSs. D. discoideum grows as a unicellular organism when food is abundant and switches from vegetative growth to multicellular development upon starvation. We found that expression of most D. discoideum TPS genes was induced during development. Upon heterologous expression, all nine TPSs from D. discoideum showed sesquiterpene synthase activities. Some also exhibited monoterpene and/or diterpene synthase activities. Direct measurement of volatile terpenes in cultures of D. discoideum revealed essentially no emission at an early stage of development. In contrast, a bouquet of terpenes, dominated by sesquiterpenes including β-barbatene and (E,E)-α-farnesene, was detected at the middle and late stages of development, suggesting a development-specific function of volatile terpenes in D. discoideum. The patchy distribution of TPS genes in the eukaryotic domain and the evidence for TPS function in D. discoideum indicate that the TPS genes mediate lineage-specific adaptations.

Keywords: amoebae; chemical ecology; evolution; terpene synthases; volatiles.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Physiological
  • Alkyl and Aryl Transferases / classification
  • Alkyl and Aryl Transferases / genetics*
  • Alkyl and Aryl Transferases / metabolism
  • Biological Evolution
  • Cloning, Molecular
  • Dictyostelium / classification
  • Dictyostelium / enzymology
  • Dictyostelium / genetics*
  • Escherichia coli / genetics
  • Escherichia coli / metabolism
  • Gene Expression
  • Gene Expression Regulation, Developmental
  • Genome, Protozoan*
  • Isoenzymes / classification
  • Isoenzymes / genetics
  • Isoenzymes / metabolism
  • Multigene Family
  • Phylogeny*
  • Protozoan Proteins / classification
  • Protozoan Proteins / genetics*
  • Protozoan Proteins / metabolism
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Terpenes / metabolism*
  • Volatilization

Substances

  • Isoenzymes
  • Protozoan Proteins
  • Recombinant Proteins
  • Terpenes
  • Alkyl and Aryl Transferases
  • terpene synthase

Associated data

  • GENBANK/KX364374
  • GENBANK/KX364382