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Reconstitution of Polyketide-Derived Meroterpenoid Biosynthetic Pathway in Aspergillus Oryzae

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Reconstitution of Polyketide-Derived Meroterpenoid Biosynthetic Pathway in Aspergillus Oryzae Journal of Fungi Review Reconstitution of Polyketide-Derived Meroterpenoid Biosynthetic Pathway in Aspergillus oryzae Takayoshi Awakawa 1,2,* and Ikuro Abe 1,2,* 1 Laboratory of Natural Products Chemistry, Graduate School of Pharmaceutical Sciences, The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan 2 Collaborative Research Institute for Innovative Microbiology, The University of Tokyo, Yayoi 1-1-1, Bunkyo-ku, Tokyo 113-8657, Japan * Correspondence: [email protected] (T.A.); [email protected] (I.A.) Abstract: The heterologous gene expression system with Aspergillus oryzae as the host is an effective method to investigate fungal secondary metabolite biosynthetic pathways for reconstruction to produce un-natural molecules due to its high productivity and genetic tractability. In this review, we focus on biosynthetic studies of fungal polyketide-derived meroterpenoids, a group of bioactive natural products, by means of the A. oryzae heterologous expression system. The heterologous expression methods and the biosynthetic reactions are described in detail for future prospects to create un-natural molecules via biosynthetic re-design. Keywords: Aspergillus oryzae; heterologous expression; secondary metabolites; meroterpenoid Citation: Awakawa, T.; Abe, I. Reconstitution of Polyketide-Derived 1. Introduction Meroterpenoid Biosynthetic Pathway Aspergillus oryzae is a fungus that has been utilized for over 2000 years in the Japanese in Aspergillus oryzae. J. Fungi 2021, 7, fermentation industry to yield sake, miso, and soy sauce, and for industrial enzyme pro- 486. https://doi.org/10.3390/jof duction. A. oryzae is an important heterologous expression host for biosynthetic genes from 7060486 Aspergillus species that produce numerous secondary metabolites, such as mycotoxins, aflatoxin, medicinal compounds, lovastatin, and pigments such as emodin [1–3], as well Academic Editors: as other secondary metabolite-producing fungi. For investigations on their biosynthesis, Katsuhiko Kitamoto and the heterologous expression system is a valuable tool, as it provides information about Yujiro Higuchi their reactions based on the products accumulated in the transformants. The A. oryzae genome includes some genes encoding secondary metabolite biosynthetic enzymes, such Received: 31 May 2021 as the non-ribosomal peptide synthetase, which is responsible for the production of toxic Accepted: 14 June 2021 compounds, such as cyclopiazonic acid. However, most of these genes, including cyclopi- Published: 16 June 2021 azonic acid synthetases, are dysfunctional or not expressed in the A. oryzae strains used in fermented food, and many have been recognized as safe strains that do not produce Publisher’s Note: MDPI stays neutral any toxic compounds [4]. In addition, A. oryzae possesses a strong metabolic flux to sup- with regard to jurisdictional claims in published maps and institutional affil- ply precursors of polyketides, terpenoids, and peptides, as judged by the high yields of iations. heterologous expression products. Furthermore, genetic manipulation methods, such as gene deletion or heterologous expression, strong promoters (e.g., PamyB and PenoA) and multicopy vectors [5,6], and the genetically tractable mutated strains A. oryzae M-2-3 and NSAR1, have been established [7,8]. The long-standing efforts of academic and industrial investigators have made this strain an excellent chassis for the heterologous expression of Copyright: © 2021 by the authors. secondary metabolite genes. By using this strain, we can easily access new biosynthetic Licensee MDPI, Basel, Switzerland. pathways and construct systems for the production of beneficial compounds. This article is an open access article distributed under the terms and The fungal meroterpenoids are one of the groups of natural products that include conditions of the Creative Commons various medicinally important compounds, such as the acyl-CoA:cholesterol acyltrans- Attribution (CC BY) license (https:// ferase inhibitor pyripyropene, the immunosuppressant mycophenolic acid, and the anti- creativecommons.org/licenses/by/ trypanosomiasis ascofuranone (Figure1)[ 9]. The biosynthesis of fungal meroterpenoids 4.0/). J. Fungi 2021, 7, 486. https://doi.org/10.3390/jof7060486 https://www.mdpi.com/journal/jof J. Fungi 2021, 7, 486 2 of 10 J.J. Fungi Fungi 2021 2021, ,7 7, ,x x FOR FOR PEER PEER REVIEW REVIEW 22 ofof 1111 cancancan be bebe separated separatedseparated into intointo five fivefive parts: parts:parts: polyketide polyketidepolyketide sy synthesis,synthesis,nthesis, prenyl prenyl transfer, transfer, epoxidation, epoxidation,epoxidation, cy- cy- clization,clization,clization, and and post-cyclization post-cyclization post-cyclization modification modification modification [10–12], [10–12], [10–12 as], as asexemplified exemplified exemplified by by bypyripyropene pyripyropene pyripyropene A A bi- bi- A osynthesisbiosynthesisosynthesis (Figure (Figure (Figure 2). 2).2). By By By using using using the the the versatile versatile A. A.A. oryzae oryzae oryzae host, host,host, which which synthesizes synthesizes polyketide polyketidepolyketide andandand terpenoid terpenoidterpenoid compounds compounds with with high high yields, yields, we we can can create create a a fungal fungal meroterpenoid meroterpenoid pro- pro- duction system. This method includes important benefits, in that we can exploit the novel ductionduction system. system. This This method method includes includes important important benefits, benefits, in in that that we we can can exploit exploit the the novel novel biocatalysts by identifying the compounds accumulated in the heterologous expression biocatalystsbiocatalysts byby identifyingidentifying thethe compoundscompounds acaccumulatedcumulated inin thethe heterologousheterologous expressionexpression system, and also re-engineer the biosynthetic pathway easily, by simply swapping one part system,system, andand alsoalso re-engineerre-engineer thethe biosyntheticbiosynthetic pathwaypathway easily,easily, byby simplysimply swappingswapping oneone of the biosynthetic machinery or feeding an un-natural substrate. partpart of of the the biosynthetic biosynthetic machinery machinery or or feeding feeding an an un-natural un-natural substrate. substrate. FigureFigureFigure 1. 1.1. Representative Representative bioactive bioactivebioactive fungal fungalfungal meroterpenoids. meroterpenoids.meroterpenoids. FigureFigureFigure 2. 2.2. Biosynthetic Biosynthetic pathway pathway of of pyripyropene pyripyropenepyripyropene A. A.A. 2. Pyripyropene A Biosynthetic Pathway 2.2. Pyripyropene Pyripyropene A A Biosynthetic Biosynthetic Pathway Pathway The earliest study of fungal meroterpenoid biosynthesis was the reconstitution of TheThe earliest earliest study study of of fungal fungal meroterpenoid meroterpenoid biosynthesis biosynthesis was was the the reconstitution reconstitution of of the the the early pyripyropene A biosynthetic pathway in the Aspergillus oryzae M-2-3Δ strain earlyearly pyripyropene pyripyropene A A biosynthetic biosynthetic pathway pathway in in the the Aspergillus Aspergillus oryzae oryzae M-2-3 M-2-3 strain strain ( (ΔargBargB)) ([13].DargB The)[13 pyr2]. The (polyketidepyr2 (polyketide synthase, synthase, PKS) gene PKS) was gene cloned was into cloned the into pTAex3 the pTAex3 vector [14], vec- [13]. The pyr2 (polyketidepyr1 synthase, PKS) gene was cloned into the pTAex3amyB vector [14], torand [14 the], andpyr1 the (CoA-ligase)(CoA-ligase) gene was gene cloned was cloned into pPTRI into pPTRI [15], with [15], withthe amyB the promoterpromoter and andand the terminator pyr1 (CoA-ligase) from pTAex3, gene to was yield cloned pTAex3- intopyr2 pPTRIand pPTRI-[15], withpyr1 the, respectively. amyB promoter Similarly, and terminator from pTAex3, to yield pTAex3-pyr2 and pPTRI-pyr1, respectively. Similarly, terminatorpyr5 (flavin-dependent from pTAex3, monooxygenase, to yield pTAex3- FMO)pyr2 wasand clonedpPTRI- intopyr1, pTAex3, respectively. and pyr4 Similarly,(trans- pyr5 (flavin-dependent monooxygenase, FMO) was cloned into pTAex3, and pyr4 (trans- pyr5membrane (flavin-dependent meroterpenoid monooxygenase, cyclase, CYC) FMO) and pyr6 was(UbiA-type cloned into prenyltransferase, pTAex3, and pyr4 PT) (trans- were membrane meroterpenoid cyclase, CYC) and pyr6 (UbiA-type prenyltransferase, PT) were membranecloned into meroterpenoid pPTRI with the cyclase,amyB promoter CYC) and and pyr6 terminator, (UbiA-type to yield prenyltransferase, pTAex3-pyr5 and PT) pPTRI- were cloned into pPTRI with the amyB promoter and terminator, to yield pTAex3-pyr5 and clonedpyr4+6 ,into respectively. pPTRI with Two the sets amyB of vectors, promoter pTAex3- and terminator,pyr2 and pPTRI- to yieldpyr1 pTAex3-and pTAex3-pyr5 pyr5and pPTRI-pyr4+6, respectively. Two sets of vectors, pTAex3-pyr2 and pPTRI-pyr1 and pPTRI-and pPTRI-pyr4+pyr46, respectively.+6, were introduced Two sets into ofAspergillus vectors, oryzaepTAex3-M-2-3pyr2 [7 ].and The pPTRI-A. oryzaepyr1/pyr1+2 and pTAex3-pyr5 and pPTRI-pyr4+6, were introduced into Aspergillus oryzae M-2-3 [7]. The A. pTAex3-was fedpyr5 nicotinic and pPTRI- acid andpyr4 produced+6, were 4-hydroxy-6-(3-pyridinyl)-2H-pyran-2-oneintroduced into Aspergillus oryzae M-2-3 [7]. (HPPO), The A. oryzae/pyr1+2 was fed nicotinic acid and produced 4-hydroxy-6-(3-pyridinyl)-2H-pyran- oryzaewhile/A.pyr1+2 oryzae was/pyr4+5+6 fed nicotinicwas fed acid HPPO and andproduced produced 4-hydroxy-6-(3-pyridinyl)-2H-pyran- deacetylpyripyropene E. The struc- 2-one
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