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

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.terpene synthases | amoebae | volatiles | evolution | chemical ecology

Airborne medicine: bacterial volatiles and their influence on plant health

“…However, mounting evidence suggests that microbes, and especially bacteria, emit diverse volatile compounds with significant biological activities on a wide range of target organisms, including plants and their pathogens (Groenhagen et al , ; Piechulla et al , ). Although plant‐associated fungi and protists also emit volatile organic compounds (Hung et al , ; Chen et al , ; Li et al , ), the present review focuses on bacterial volatiles and highlights the diverse means by which these compounds contribute to maintaining and protecting plant health.…”

A detailed view on 1,8-cineol biosynthesis by Streptomyces clavuligerus

“…An estimated number of 75,000 different compounds are known from all kinds of organisms including plants [1], bacteria [2–5], fungi [6] and, as recently shown, even social amoebae [7]. These molecules are all made from only a handful of linear and achiral precursors such as geranyl diphosphate (GPP, monoterpenes), farnesyl diphosphate (FPP, sesquiterpenes) and geranylgeranyl diphosphate (GGPP, diterpenes).…”

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“…They are best known to humans as plants metabolites. However, recent studies revealed that terpenes can be produced by all kingdoms of life including prokaryotes (Takamatsu et al 2011;Yamada et al 2012;Yamada et al 2015;Song et al 2015b;Chen et al 2016). Recently, Yamada et al (2015) described a powerful bioinformatics method based on the use of Hidden Markov Models (HMMs) and Protein Families Database (PFAM) search that has allowed the discovery of terpene synthases of bacterial origin and showed that phylogenetically different bacteria can be a rich source of terpenes.…”

“…In this context, terpenes as one of the largest and most diverse class of metabolites that are produced by all kingdom of live including bacteria, fungi and plants (this thesis; Yamada et al 2015;Chen et al 2016) seem to play important roles in many soil processes (Chapter 2). For instance, terpene-mediated interactions can contribute to the suppression of soil-borne plant diseases (Song et al 2015b; Chapter 6), stimulation of plant growth (Minerdi et al 2011), soil nutrient cycles (Kleinheinz et al 1999;Owen et al 2007; Chapter 3), or the connection of soil food webs (Chapter 4).…”

“…Recently Chen et al (2016) revealed that protists such as Dictyostelium discoideum produce terpenes, which might be involved in defense mechanisms, for example, to repel nematodes. However, since protists similar as fungi (Chapter 5) are probably never alone, the question arises if and in which way associated bacteria would be involved in the production of VOCs such as terpenes by protists.…”