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

Jia, Qidong; Chen, Xinlu; Köllner, Tobias G.; Rinkel, Jan; Fu, Jianyu; Labbé, Jessy; Xiong, Wangdan; Dickschat, Jeroen S.; Gershenzon, Jonathan; Chen, Feng

doi:10.1038/s41598-019-45532-1

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

Journal Article · Tue Jun 25 00:00:00 EDT 2019 · Scientific Reports

DOI:https://doi.org/10.1038/s41598-019-45532-1· OSTI ID:1545189

Jia, Qidong ^[1];

^[2];

^[3]; Rinkel, Jan ^[4]; Fu, Jianyu ^[5];

^[6]; Xiong, Wangdan ^[2]; Dickschat, Jeroen S. ^[4]; Gershenzon, Jonathan ^[3];

^[2]

Univ. of Tennessee, Knoxville, TN (United States); Univ. of Nebraska, Lincoln, NE (United States)
Univ. of Tennessee, Knoxville, TN (United States)
Max Planck Society, Jena (Germany)
Univ. of Bonn (Germany)
Chinese Academy of Agricultural Sciences, Hangzhou (China)
Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Nebraska, Lincoln, NE (United States)

Fungi are essential eukaryotes of wide distribution. They are known as rich producers of secondary metabolites, especially terpenoids, which are crucial for fungi-environment interactions. Horizontal gene transfer (HGT) is an important mechanism contributing to genetic innovation of fungi. Yet, 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.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1545189

Journal Information:: Scientific Reports, Vol. 9, Issue 1; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 22 works

Citation information provided by
Web of Science

References (47)

Molecular Basis for Stellatic Acid Biosynthesis: A Genome Mining Approach for Discovery of Sesterterpene Synthases Matsuda, Yudai; Mitsuhashi, Takaaki; Quan, Zhiyang Organic Letters, Vol. 17, Issue 18 https://doi.org/10.1021/acs.orglett.5b02404	journal	September 2015
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
Plant P450s as versatile drivers for evolution of species-specific chemical diversity Hamberger, Björn; Bak, Søren Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1612 https://doi.org/10.1098/rstb.2012.0426	journal	February 2013
PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments Suyama, M.; Torrents, D.; Bork, P. Nucleic Acids Research, Vol. 34, Issue Web Server https://doi.org/10.1093/nar/gkl315	journal	July 2006
The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom: Terpene synthase family Chen, Feng; Tholl, Dorothea; Bohlmann, Jörg The Plant Journal, Vol. 66, Issue 1 https://doi.org/10.1111/j.1365-313X.2011.04520.x	journal	March 2011
ProtTest 3: fast selection of best-fit models of protein evolution Darriba, Diego; Taboada, Guillermo L.; Doallo, Ramón Bioinformatics, Vol. 27, Issue 8 https://doi.org/10.1093/bioinformatics/btr088	journal	February 2011
Genome-Based Discovery of an Unprecedented Cyclization Mode in Fungal Sesterterpenoid Biosynthesis Okada, Masahiro; Matsuda, Yudai; Mitsuhashi, Takaaki Journal of the American Chemical Society, Vol. 138, Issue 31 https://doi.org/10.1021/jacs.6b05799	journal	August 2016
Mathematical Modeling of Evolution of Horizontally Transferred Genes Novozhilov, A. S. Molecular Biology and Evolution, Vol. 22, Issue 8 https://doi.org/10.1093/molbev/msi167	journal	April 2005
Fungal secondary metabolism — from biochemistry to genomics Keller, Nancy P.; Turner, Geoffrey; Bennett, Joan W. Nature Reviews Microbiology, Vol. 3, Issue 12, p. 937-947 https://doi.org/10.1038/nrmicro1286	journal	December 2005
Lessons from 1,3-Hydride Shifts in Sesquiterpene Cyclizations Rinkel, Jan; Rabe, Patrick; Garbeva, Paolina Angewandte Chemie International Edition, Vol. 55, Issue 43 https://doi.org/10.1002/anie.201608042	journal	September 2016
Bacterial–fungal interactions: ecology, mechanisms and challenges Deveau, Aurélie; Bonito, Gregory; Uehling, Jessie FEMS Microbiology Reviews, Vol. 42, Issue 3 https://doi.org/10.1093/femsre/fuy008	journal	February 2018
Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences Li, W.; Godzik, A. Bioinformatics, Vol. 22, Issue 13 https://doi.org/10.1093/bioinformatics/btl158	journal	May 2006
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0 Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent Systematic Biology, Vol. 59, Issue 3 https://doi.org/10.1093/sysbio/syq010	journal	March 2010
Chemistry and Biology of Mycotoxins and Related Fungal Metabolites Bräse, Stefan; Encinas, Arantxa; Keck, Julia Chemical Reviews, Vol. 109, Issue 9 https://doi.org/10.1021/cr050001f	journal	September 2009
Identification of Ophiobolin F Synthase by a Genome Mining Approach: A Sesterterpene Synthase from Aspergillus clavatus Chiba, Ryota; Minami, Atsushi; Gomi, Katsuya Organic Letters, Vol. 15, Issue 3 https://doi.org/10.1021/ol303408a	journal	January 2013
Fungal—bacterial interactions: a mixed bag of mingling microbes Wargo, Matthew J.; Hogan, Deborah A. Current Opinion in Microbiology, Vol. 9, Issue 4 https://doi.org/10.1016/j.mib.2006.06.001	journal	August 2006
Astellifadiene: Structure Determination by NMR Spectroscopy and Crystalline Sponge Method, and Elucidation of its Biosynthesis Matsuda, Yudai; Mitsuhashi, Takaaki; Lee, Shoukou Angewandte Chemie International Edition, Vol. 55, Issue 19 https://doi.org/10.1002/anie.201601448	journal	April 2016
Mauve: Multiple Alignment of Conserved Genomic Sequence With Rearrangements Darling, A. C. E. Genome Research, Vol. 14, Issue 7 https://doi.org/10.1101/gr.2289704	journal	June 2004
Genome Mining for Sesterterpenes Using Bifunctional Terpene Synthases Reveals a Unified Intermediate of Di/Sesterterpenes Ye, Ying; Minami, Atsushi; Mandi, Attila Journal of the American Chemical Society, Vol. 137, Issue 36 https://doi.org/10.1021/jacs.5b08319	journal	September 2015
Structures and Biosynthesis of Corvol Ethers-Sesquiterpenes from the Actinomycete Kitasatospora setae Rabe, Patrick; Pahirulzaman, Khomaizon A. K.; Dickschat, Jeroen S. Angewandte Chemie International Edition, Vol. 54, Issue 20 https://doi.org/10.1002/anie.201501119	journal	March 2015
Fungal volatile compounds induce production of the secondary metabolite Sodorifen in Serratia plymuthica PRI-2C Schmidt, Ruth; Jager, Victor de; Zühlke, Daniela Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-00893-3	journal	April 2017
Terpene synthases are widely distributed in bacteria Yamada, Yuuki; Kuzuyama, Tomohisa; Komatsu, Mamoru Proceedings of the National Academy of Sciences, Vol. 112, Issue 3 https://doi.org/10.1073/pnas.1422108112	journal	December 2014
The fate of laterally transferred genes: Life in the fast lane to adaptation or death Hao, W. Genome Research, Vol. 16, Issue 5 https://doi.org/10.1101/gr.4746406	journal	May 2006
Hyphal morphogenesis: an evolutionary perspective Harris, Steven D. Fungal Biology, Vol. 115, Issue 6 https://doi.org/10.1016/j.funbio.2011.02.002	journal	June 2011
Pfam: the protein families database Finn, Robert D.; Bateman, Alex; Clements, Jody Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1223	journal	November 2013
FastML: a web server for probabilistic reconstruction of ancestral sequences Ashkenazy, H.; Penn, O.; Doron-Faigenboim, A. Nucleic Acids Research, Vol. 40, Issue W1 https://doi.org/10.1093/nar/gks498	journal	May 2012
An Unusual Chimeric Diterpene Synthase from Emericella variecolor and Its Functional Conversion into a Sesterterpene Synthase by Domain Swapping Qin, Bin; Matsuda, Yudai; Mori, Takahiro Angewandte Chemie International Edition, Vol. 55, Issue 5 https://doi.org/10.1002/anie.201509263	journal	November 2015
An Improved Technique for the Rapid Chemical Characterisation of Bacterial Terpene Cyclases Dickschat, Jeroen S.; Pahirulzaman, Khomaizon A. K.; Rabe, Patrick ChemBioChem, Vol. 15, Issue 6 https://doi.org/10.1002/cbic.201300763	journal	February 2014
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
Large-scale high-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method Gietz, R. Daniel; Schiestl, Robert H. Nature Protocols, Vol. 2, Issue 1 https://doi.org/10.1038/nprot.2007.15	journal	January 2007
Comprehensive curation and analysis of fungal biosynthetic gene clusters of published natural products Li, Yong Fuga; Tsai, Kathleen J. S.; Harvey, Colin J. B. Fungal Genetics and Biology, Vol. 89 https://doi.org/10.1016/j.fgb.2016.01.012	journal	April 2016
jModelTest 2: more models, new heuristics and parallel computing Darriba, Diego; Taboada, Guillermo L.; Doallo, Ramón Nature Methods, Vol. 9, Issue 8 https://doi.org/10.1038/nmeth.2109	journal	July 2012
Frequent, independent transfers of a catabolic gene from bacteria to contrasted filamentous eukaryotes Bruto, Maxime; Prigent-Combaret, Claire; Luis, Patricia Proceedings of the Royal Society B: Biological Sciences, Vol. 281, Issue 1789 https://doi.org/10.1098/rspb.2014.0848	journal	August 2014
Astellifadiene: Structure Determination by NMR Spectroscopy and Crystalline Sponge Method, and Elucidation of its Biosynthesis Matsuda, Yudai; Mitsuhashi, Takaaki; Lee, Shoukou Angewandte Chemie, Vol. 128, Issue 19 https://doi.org/10.1002/ange.201601448	journal	April 2016
Systematic discovery of pseudomonad genetic factors involved in sensitivity to tailocins Carim, Sean; Azadeh, Ashley L.; Kazakov, Alexey E. The ISME Journal, Vol. 15, Issue 8 https://doi.org/10.1038/s41396-021-00921-1	journal	March 2021
FastML: a web server for probabilistic reconstruction of ancestral sequences Ashkenazy, H.; Penn, O.; Doron-Faigenboim, A. Oxford University Press https://doi.org/10.7892/boris.16913	text	January 2012
An Unusual Chimeric Diterpene Synthase from Emericella variecolor and Its Functional Conversion into a Sesterterpene Synthase by Domain Swapping Qin, Bin; Matsuda, Yudai; Mori, Takahiro Angewandte Chemie, Vol. 128, Issue 5 https://doi.org/10.1002/ange.201509263	journal	November 2015
New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0 Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent Oxford University Press https://doi.org/10.5167/uzh-155669	text	January 2010
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, A. Karlsruhe https://doi.org/10.5445/ir/1000045818	text	January 2014
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0 Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent ETH Zurich https://doi.org/10.3929/ethz-b-000025281	text	January 2010
Mathematical modeling of evolution of horizontally transferred genes Novozhilov, Artem S.; Karev, Georgy P.; Koonin, Eugene V. arXiv https://doi.org/10.48550/arxiv.q-bio/0509010	preprint	January 2005
Mating pair stabilization mediates bacterial conjugation species specificity Low, Wen Wen; Wong, Joshua L. C.; Beltran, Leticia C. Nature Microbiology, Vol. 7, Issue 7 https://doi.org/10.1038/s41564-022-01146-4	journal	June 2022
Microevolution of Campylobacter jejuni during long-term infection in an immunocompromised host Barker, Clare R.; Painset, Anaïs; Swift, Craig Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-66771-7	journal	June 2020
Full-length transcriptome analysis of multiple organs and identification of adaptive genes and pathways in Mikania micrantha Ruan, Xiaoxian; Wang, Zhen; Su, Yingjuan Scientific Reports, Vol. 12, Issue 1 https://doi.org/10.1038/s41598-022-07198-0	journal	February 2022
Traversing the fungal terpenome Quin, Maureen B.; Flynn, Christopher M.; Schmidt-Dannert, Claudia Nat. Prod. Rep., Vol. 31, Issue 10 https://doi.org/10.1039/c4np00075g	journal	January 2014
Bacterial terpene cyclases Dickschat, Jeroen S. Natural Product Reports, Vol. 33, Issue 1 https://doi.org/10.1039/c5np00102a	journal	January 2016
Relationship between Secondary Metabolism and Fungal Development Calvo, A. M.; Wilson, R. A.; Bok, J. W. Microbiology and Molecular Biology Reviews, Vol. 66, Issue 3 https://doi.org/10.1128/mmbr.66.3.447-459.2002	journal	September 2002

Cited By (3)

Mechanistic Studies on Trichoacorenol Synthase from Amycolatopsis benzoatilytica Rinkel, Jan; Dickschat, Jeroen S. ChemBioChem, Vol. 21, Issue 6 https://doi.org/10.1002/cbic.201900584	journal	November 2019
Hitherto Unknown Terpene Synthase Organization in Taxol-Producing Endophytic Bacteria Isolated from Marine Macroalgae Subramanian, Mugesh; Marudhamuthu, Murugan Current Microbiology, Vol. 77, Issue 6 https://doi.org/10.1007/s00284-020-01878-8	journal	January 2020
Emission and biosynthesis of volatile terpenoids from the plasmodial slime mold Physarum polycephalum Chen, Xinlu; Köllner, Tobias G.; Xiong, Wangdan Beilstein Journal of Organic Chemistry, Vol. 15 https://doi.org/10.3762/bjoc.15.281	journal	January 2019

Similar Records

Terpene Synthases as Metabolic Gatekeepers in the Evolution of Plant Terpenoid Chemical Diversity

Journal Article · Tue Oct 01 00:00:00 EDT 2019 · Frontiers in Plant Science · OSTI ID:1545189

Karunanithi, Prema S.; Zerbe, Philipp

Microbial-type terpene synthase genes occur widely in nonseed land plants, but not in seed plants

Journal Article · Mon Oct 10 00:00:00 EDT 2016 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1545189

Jia, Qidong; Li, Guanglin; Köllner, Tobias G.; +17 more

Genome-Wide Analysis of Terpene Synthase Gene Family in Mentha longifolia and Catalytic Activity Analysis of a Single Terpene Synthase

Journal Article · Fri Apr 02 00:00:00 EDT 2021 · Genes · OSTI ID:1545189

Chen, Zequn; Vining, Kelly; Qi, Xiwu; +9 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

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

Citation Formats

References (47)

Cited By (3)

Similar Records

Related Subjects