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Terpene Synthase Genes in Eukaryotes Beyond Plants and Fungi: Occurrence in Social Amoebae

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Terpene Synthase Genes in Eukaryotes Beyond Plants and Fungi: Occurrence in Social Amoebae Terpene synthase genes in eukaryotes beyond plants and fungi: Occurrence in social amoebae Xinlu Chena, Tobias G. Köllnerb, Qidong Jiac, Ayla Norrisc, Balaji Santhanamd,e, Patrick Rabef, Jeroen S. Dickschatf, Gad Shaulskye, Jonathan Gershenzonb, and Feng Chena,c,1 aDepartment of Plant Sciences, University of Tennessee, Knoxville, TN 37996; bDepartment of Biochemistry, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany; cGraduate School of Genome Science and Technology, University of Tennessee, Knoxville, TN 37996; dGraduate Program in Structural Computational Biology and Molecular Biophysics, Baylor College of Medicine, Houston, TX 77030; eDepartment of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030; and fKekulé-Institute of Organic Chemistry and Biochemistry, University of Bonn, 53121 Bonn, Germany Edited by Jerrold Meinwald, Cornell University, Ithaca, NY, and approved August 30, 2016 (received for review June 27, 2016) Terpenes are structurally diverse natural products involved in many the IDS-type terpene synthases have been identified recently in ecological interactions. The pivotal enzymes for terpene biosynthe- two species of insects (11, 12). Sequence analysis of these insect sis, terpene synthases (TPSs), had been described only in plants and genes suggests that they have evolved recently from insect IDSs fungi in the eukaryotic domain. In this report, we systematically (12), whereas classic TPSs probably also evolved from IDSs, but analyzed the genome sequences of a broad range of nonplant/ anciently (13). TPS genes are major contributors to the chemical TPS nonfungus eukaryotes and identified putative genes in six spe- diversity exhibited by living organisms, so it is important to un- cies of amoebae, five of which are multicellular social amoebae derstand their distribution and evolution. from the order of Dictyosteliida. A phylogenetic analysis revealed In the current global tree of eukaryotes, a domain that is that amoebal TPSs are evolutionarily more closely related to fungal composed of diverse organisms, the five supergroups Opistho- TPSs than to bacterial TPSs. The social amoeba Dictyostelium discoideum konta, Amoebozoa, Excavata, Archaeplastida, and SAR (stra- was selected for functional study of the identified TPSs. + + D. discoideum grows as a unicellular organism when food is abun- menopiles alveolates Rhizaria) are recognized (14, 15). Only dant and switches from vegetative growth to multicellular devel- the supergroup Archaeplastida, which contains land plants, and opment upon starvation. We found that expression of most Opisthokonta, which contains fungi, are known to contain classic D. discoideum TPS genes was induced during development. Upon TPS genes. It has been accepted that classic TPS genes are ab- heterologous expression, all nine TPSs from D. discoideum showed sent in insects (12), which are in the supergroup of Opistho- sesquiterpene synthase activities. Some also exhibited monoter- konta. The presence/absence of TPS genes in other eukaryotes pene and/or diterpene synthase activities. Direct measurement of has not been systematically investigated. Terpenes serve diverse volatile terpenes in cultures of D. discoideum revealed essentially no functions in the organisms that produce them, including defense emission at an early stage of development. In contrast, a bouquet of against predators and attraction of beneficial organisms (16), terpenes, dominated by sesquiterpenes including β-barbatene and which implies that TPS genes play a role in evolutionary adap- E E α ( , )- -farnesene, was detected at the middle and late stages of de- tations. The goals of this study were to systematically search for velopment, suggesting a development-specific function of volatile classic TPS genes in nonplant/nonfungus eukaryotes, infer their terpenes in D. discoideum. The patchy distribution of TPS genes in evolutionary relationship to known TPSs, and understand their the eukaryotic domain and the evidence for TPS function in biochemical and biological functions. D. discoideum indicate that the TPS genes mediate lineage-specific adaptations. Significance terpene synthases | amoebae | volatiles | evolution | chemical ecology Many living organisms use terpenes for ecological interactions. erpenes constitute a structurally diverse class of natural Terpenes are biosynthesized by terpene synthases (TPSs), but TPS products. They are synthesized from two universal precursors: classic genes are known to exist only in plants and fungi T TPS isopentenyl diphosphate (IPP) and dimethylallyl diphosphate among the eukaryotes. In this study, genes were identified (DMAPP), which are supplied by the mevalonate pathway and/or in six species of amoebae with five of them being multicellular the methylerythritol phosphate pathway (1). From IPP and DMAPP, social amoebae. Amoebal TPSs showed closer relatedness to Dictyos- isoprenyl diphosphates of various chain lengths are produced by the fungal TPSs than bacterial TPSs. In the social amoeba telium discoideum TPS action of isoprenyl diphosphate synthases (IDSs) (2). Among the , all nine genes encoded active enzymes many metabolic fates of isoprenyl diphosphates (3), they serve as and most of their terpene products were released as volatiles substrates for terpene synthases, which convert isoprenyl diphos- in a development-specific manner. This study highlights a TPS phates to different subclasses of terpenes of fascinating structural wider distribution of genes in eukaryotes than previously diversity, such as monoterpenes, sesquiterpenes, and diterpenes thought and opens a door to studying the function and evo- TPS (4). The ability of an organism to produce terpenes depends on lution of genes and their products. whether the organism contains terpene synthase genes. Author contributions: X.C., T.G.K., J.S.D., G.S., J.G., and F.C. designed research; X.C., T.G.K., Unlike IDS genes, which are ubiquitous in living organisms, Q.J., A.N., B.S., and P.R. performed research; X.C., T.G.K., Q.J., J.S.D., G.S., J.G., and F.C. the occurrence of terpene synthase genes and, thus, the pro- analyzed data; and X.C., T.G.K., J.S.D., G.S., J.G., and F.C. wrote the paper. duction of terpenes appear to be lineage-specific. Presently, two The authors declare no conflict of interest. general types of terpene synthases are recognized: classic terpene This article is a PNAS Direct Submission. synthases (abbreviated as TPSs) and IDS-type terpene synthases. Data deposition: The sequences for the biochemically characterized terpene synthases The majority of terpene synthases that have been characterized reported in this paper have been deposited in the GenBank database (accession nos. so far belongs to the classic TPSs. In prokaryotes, classic TPS KX364374–KX364382). genes are widely distributed in bacteria (5, 6), whereas none has 1To whom correspondence should be addressed. Email: [email protected]. been observed in archaea. In eukaryotes, classic TPS genes had This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. been found only in land plants (7, 8) and fungi (9, 10), whereas 1073/pnas.1610379113/-/DCSupplemental. 12132–12137 | PNAS | October 25, 2016 | vol. 113 | no. 43 www.pnas.org/cgi/doi/10.1073/pnas.1610379113 Downloaded by guest on October 2, 2021 Land plants NA Identified Eukaryotic Terpene Synthases: Evolutionary Relatedness ArchaeplasƟda and Motifs. To understand the evolutionary relatedness of the Green algae 0/10 identified eukaryotic TPSs with known TPSs, a phylogenetic tree Red algae 0/3 was constructed that includes, besides the eukaryotic TPSs de- scribed here, representative bacterial and fungal TPSs, and mi- SAR Stramenopiles 0/7 crobial type TPSs from the lycophyte Selaginella moellendorffii Alveolata 0/19 (8). Notably, the TPSs from the five species of Dictyosteliida Excavata Eukaryotes Excavates 1/10 clustered together (clade I), whereas the seven TPSs from Dictyosteliida 3/3 +2 N. gruberi clustered in a separate, but closely related clade (clade Amoebozoa II) (Fig. 2). Together, the amoebal TPSs showed closer relatedness Entamoeba 0/3 to fungal TPSs than to bacterial TPSs (Fig. 2). Acanthamoeba 0/1 TPSs contain several highly conserved motifs that are important for catalytic activity including the aspartate-rich “DDxx(x)D/E” Opisthokonta Holomycota NA motif and the “NDxxSxxxD/E” motif, both of which are involved in Holozoa 0/112 complexing metal ions to coordinate the binding of the isoprenyl diphosphate substrate in the active site (20, 21). Both motifs are also Fig. 1. Distribution of terpene synthase (TPS) genes among the major lineages of eukaryotes with sequenced genomes. A total of 168 species highly conserved among all newly identified eukaryotic TPSs (Table (Table S1), which did not include any species from land plants and fungi S3). In addition, the diphosphate sensor that is involved in substrate (Holomycota), were analyzed. The phylogeny of eukaryotes was adapted recognition and critical for catalytic activity (Arginine) (6, 22) was from Adl et al. (14) and Burki (15) with five supergroups recognized: Opis- also highly conserved (Table S3). thokonta, Amoebozoa, Excavata, Archaeplastida, and SAR (stramenopiles + alveolates + Rhizaria). The first number (before the slash) indicates the Expression Patterns of Individual Terpene Synthase Genes in Dictyostelium number of species in certain lineages that were determined to contain TPS discoideum. D. discoideum was selected as a model system to explore
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