Terpene Synthase Genes Originated from Bacteria through Horizontal Gene Transfer Contribute to Terpenoid Diversity in Fungi

Authors

Qidong Jia, University of Nebraska - LincolnFollow
Xinlu Chen, University of Tennessee, Knoxville
Tobias G. Kollner, Max Planck Institute for Chemical Ecology
Jan Rinkel, University of Bonn
Jianyu Fu, Chinese Academy of Agricultural Sciences
Jessy Labbe, University of Tennessee, Knoxville
Wangdan Xiong, University of Tennessee, Knoxville
Jeroen S. Dickschat, University of Bonn
Jonathan Gershenzon, Max Planck Institute for Chemical Ecology
Feng Chen, University of Tennessee, KnoxvilleFollow

ORCID IDs

0000-0002-7560-6125

0000-0002-7037-904X

0000-0003-0368-2054

0000-0002-3267-4646

Document Type

Article

Date of this Version

2019

Citation

Scientific Reports | (2019) 9:9223

Comments

© The Author(s) 2019

Open access

https://doi.org/10.1038/s41598-019-45532-1

Abstract

Fungi are successful eukaryotes of wide distribution. They are known as rich producers of secondary metabolites, especially terpenoids, which are important for fungi-environment interactions. Horizontal gene transfer (HGT) is an important mechanism contributing to genetic innovation of fungi. However, it remains unclear whether HGT has played a role in creating the enormous chemical diversity of fungal terpenoids. Here we report that fungi have acquired terpene synthase genes (TPSs), which encode pivotal enzymes for terpenoid biosynthesis, from bacteria through HGT. Phylogenetic analysis placed the majority of fungal and bacterial TPS genes from diverse taxa into two clades, indicating ancient divergence. Nested in the bacterial TPS clade is a number of fungal TPS genes that are inferred as the outcome of HGT. These include a monophyletic clade of nine fungal TPS genes, designated as BTPSL for bacterial TPS-like genes, from eight species of related entomopathogenic fungi, including seven TPSs from six species in the genus Metarhizium. In vitro enzyme assays demonstrate that all seven BTPSL genes from the genus Metarhizium encode active enzymes with sesquiterpene synthase activities of two general product profiles. By analyzing the catalytic activity of two resurrected ancestral BTPSLs and one closely related bacterial TPS, the trajectory of functional evolution of BTPSLs after HGT from bacteria to fungi and functional divergence within Metarhizium could be traced. Using M. brunneum as a model species, both BTPSLs and typical fungal TPSs were demonstrated to be involved in the in vivo production of terpenoids, illustrating the general importance of HGT of TPS genes from bacteria as a mechanism contributing to terpenoid diversity in fungi.