Major involvement of two laccase genes in conidial pigment biosynthesis in Aspergillus oryzae

Tamano, Koichi; Takayama, Haruka; Yasokawa, Saeko; Sano, Motoaki; Baker, Scott E.

doi:10.1007/s00253-021-11669-1

Major involvement of two laccase genes in conidial pigment biosynthesis in Aspergillus oryzae

Journal Article · Fri Dec 10 00:00:00 EST 2021 · Applied Microbiology and Biotechnology

DOI:https://doi.org/10.1007/s00253-021-11669-1· OSTI ID:1841744

^[1]; Takayama, Haruka ^[2]; Yasokawa, Saeko ^[2]; Sano, Motoaki ^[3]; ^[4]

National Inst. of Advanced Industrial Science and Technology (AIST), Hokkaido (Japan); Waseda Univ., Shinjuku (Japan)
National Inst. of Advanced Industrial Science and Technology (AIST), Hokkaido (Japan)
Kanazawa Institute of Technology (Japan)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)

Wild-type strains of Aspergillus oryzae develop yellow, yellow-green, green, or brown conidia. Previous reports suggested that the conidiation initiates with the biosynthesis of a yellow pigment YWA1 from acetyl-CoA by a polyketide synthase encoded by wA (AO090102000545). This is followed by the conversion to other pigment by a laccase encoded by yA (AO090011000755). Based on orthologous pathways in other aspergilli, it is reasonable to hypothesize that in addition to yA, AO090102000546 encoding laccase and AO090005000332 encoding Ayg1-like hydrolase play a role in A. oryzae conidial pigment biosynthesis. However, the involvement of these two genes in conidial pigmentation remains unclear. In this study, we tested this hypothesis by assessing the conidial colors of both disruption and overexpression mutants to verify whether AO090102000546 and AO090005000332 were associated with the conidial pigmentation. Here, observation of single, double, and triple disruptants of these three genes suggested that conidial pigments were synthesized by two laccase genes, AO090011000755 and AO090102000546, whereas Ayg1-like hydrolase gene AO090005000332 was proven to have no obvious association with the synthesis. This was corroborated by observing the phenotype of each overexpression mutant. Interestingly, AO090005000332 overexpression mutant produced smoky yellow-green conidia, different from the wild-type strain. Thus, the AO090005000332-encoded protein is likely to maintain the enzymatic activity. However, the expression level was observed to be one-third of that of AO090102000546 and one-seventh of that of AO090011000755. Consequently, apparent lack of obvious contribution of AO090005000332 to conidial pigmentation could be attributed to its low expression level. Expression analysis indicated similar profiles in several wild-type strains.

View Accepted Manuscript (DOE)

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1841744

Report Number(s):: PNNL-SA--168546

Journal Information:: Applied Microbiology and Biotechnology, Journal Name: Applied Microbiology and Biotechnology Journal Issue: 1 Vol. 106; ISSN 0175-7598

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

References (26)

On the safety of Aspergillus oryzae: a review Barbesgaard, Peder; Heldt-Hansen, HansPeter; Diderichsen, B�rge Applied Microbiology and Biotechnology, Vol. 36, Issue 5 https://doi.org/10.1007/BF00183230	journal	February 1992
Increased production of fatty acids and triglycerides in Aspergillus oryzae by enhancing expressions of fatty acid synthesis-related genes Tamano, Koichi; Bruno, Kenneth S.; Karagiosis, Sue A. Applied Microbiology and Biotechnology, Vol. 97, Issue 1 https://doi.org/10.1007/s00253-012-4193-y	journal	June 2012
Safety of the fungal workhorses of industrial biotechnology: update on the mycotoxin and secondary metabolite potential of Aspergillus niger, Aspergillus oryzae, and Trichoderma reesei Frisvad, Jens C.; Møller, Lars L. H.; Larsen, Thomas O. Applied Microbiology and Biotechnology, Vol. 102, Issue 22 https://doi.org/10.1007/s00253-018-9354-1	journal	October 2018
Identification of a copper-transporting ATPase involved in biosynthesis of A. flavus conidial pigment Chang, Perng-Kuang; Scharfenstein, Leslie L.; Mack, Brian Applied Microbiology and Biotechnology, Vol. 103, Issue 12 https://doi.org/10.1007/s00253-019-09820-0	journal	April 2019
Biosynthesis of conidial and sclerotial pigments in Aspergillus species Chang, Perng-Kuang; Cary, Jeffrey W.; Lebar, Matthew D. Applied Microbiology and Biotechnology, Vol. 104, Issue 6 https://doi.org/10.1007/s00253-020-10347-y	journal	January 2020
Utilization of the TEF1-a gene ( TEF1 ) promoter for expression of polygalacturonase genes, pgaA and pgaB , in Aspergillus oryzae Kitamoto, N.; Matsui, J.; Kawai, Y. Applied Microbiology and Biotechnology, Vol. 50, Issue 1 https://doi.org/10.1007/s002530051260	journal	July 1998
Enhanced gene targeting frequency in ku70 and ku80 disruption mutants of Aspergillus sojae and Aspergillus oryzae Takahashi, Tadashi; Masuda, Tsutomu; Koyama, Yasuji Molecular Genetics and Genomics, Vol. 275, Issue 5 https://doi.org/10.1007/s00438-006-0104-1	journal	February 2006
Development of a genome editing technique using the CRISPR/Cas9 system in the industrial filamentous fungus Aspergillus oryzae Katayama, Takuya; Tanaka, Yuki; Okabe, Tomoya Biotechnology Letters, Vol. 38, Issue 4 https://doi.org/10.1007/s10529-015-2015-x	journal	December 2015
Re-identification of Aspergillus nidulans wA gene to code for a polyketide synthase of naphthopyrone Watanabe, Akira; Fujii, Isao; Sankawa, Ushio Tetrahedron Letters, Vol. 40, Issue 1 https://doi.org/10.1016/S0040-4039(98)80027-0	journal	January 1999
Transcriptional regulation of genes on the non-syntenic blocks of Aspergillus oryzae and its functional relationship to solid-state cultivation Tamano, Koichi; Sano, Motoaki; Yamane, Noriko Fungal Genetics and Biology, Vol. 45, Issue 2 https://doi.org/10.1016/j.fgb.2007.09.005	journal	February 2008
A defect of LigD (human Lig4 homolog) for nonhomologous end joining significantly improves efficiency of gene-targeting in Aspergillus oryzae Mizutani, Osamu; Kudo, Youhei; Saito, Akemi Fungal Genetics and Biology, Vol. 45, Issue 6 https://doi.org/10.1016/j.fgb.2007.12.010	journal	June 2008
Characterization of a polyketide synthase in Aspergillus niger whose product is a precursor for both dihydroxynaphthalene (DHN) melanin and naphtho-γ-pyrone Chiang, Yi-Ming; Meyer, Kristen M.; Praseuth, Michael Fungal Genetics and Biology, Vol. 48, Issue 4 https://doi.org/10.1016/j.fgb.2010.12.001	journal	April 2011
The molecular and genetic basis of conidial pigmentation in Aspergillus niger Jørgensen, Thomas R.; Park, Joohae; Arentshorst, Mark Fungal Genetics and Biology, Vol. 48, Issue 5 https://doi.org/10.1016/j.fgb.2011.01.005	journal	May 2011
Penicillin biosynthesis in Aspergillus oryzae and its overproduction by genetic engineering Marui, Junichiro; Ohashi-Kunihiro, Sumiko; Ando, Tomohiro Journal of Bioscience and Bioengineering, Vol. 110, Issue 1 https://doi.org/10.1016/j.jbiosc.2010.01.001	journal	July 2010
Development and refinement of a high-efficiency gene-targeting system for Aspergillus flavus Chang, Perng-Kuang; Scharfenstein, Leslie L.; Wei, Qijian Journal of Microbiological Methods, Vol. 81, Issue 3 https://doi.org/10.1016/j.mimet.2010.03.010	journal	June 2010
Production of toxic metabolites in Aspergillus niger, Aspergillus oryzae, and Trichoderma reesei: justification of mycotoxin testing in food grade enzyme preparations derived from the three fungi Blumenthal, Cynthia Z. Regulatory Toxicology and Pharmacology, Vol. 39, Issue 2 https://doi.org/10.1016/j.yrtph.2003.09.002	journal	April 2004
Genome sequencing and analysis of Aspergillus oryzae Machida, Masayuki; Asai, Kiyoshi; Sano, Motoaki Nature, Vol. 438, Issue 7071 https://doi.org/10.1038/nature04300	journal	December 2005
A structural-chemical explanation of fungal laccase activity Mehra, Rukmankesh; Muschiol, Jan; Meyer, Anne S. Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-35633-8	journal	November 2018
From The Cover: Highly efficient gene replacements in Neurospora strains deficient for nonhomologous end-joining Ninomiya, Y.; Suzuki, K.; Ishii, C. Proceedings of the National Academy of Sciences, Vol. 101, Issue 33 https://doi.org/10.1073/pnas.0402780101	journal	August 2004
Nonhomologous chromosomal integration of foreign DNA is completely dependent on MUS-53 (human Lig4 homolog) in Neurospora Ishibashi, K.; Suzuki, K.; Ando, Y. Proceedings of the National Academy of Sciences, Vol. 103, Issue 40 https://doi.org/10.1073/pnas.0604477103	journal	September 2006
Pentaketide Melanin Biosynthesis in Aspergillus fumigatus Requires Chain-length Shortening of a Heptaketide Precursor Tsai, Huei-Fung; Fujii, Isao; Watanabe, Akira Journal of Biological Chemistry, Vol. 276, Issue 31 https://doi.org/10.1074/jbc.M101998200	journal	May 2001
Simple procedure for disruption of fungal spores Van Etten, J. L.; Freer, S. N. Applied and Environmental Microbiology, Vol. 35, Issue 3 https://doi.org/10.1128/aem.35.3.622-623.1978	journal	March 1978
Use of the kojA promoter, involved in kojic acid biosynthesis, for polyketide production in Aspergillus oryzae: implications for long-term production Tamano, Koichi; Kuninaga, Mahoko; Kojima, Naoshi BMC Biotechnology, Vol. 19, Issue 1 https://doi.org/10.1186/s12896-019-0567-x	journal	October 2019
The β-1,3-Exoglucanase Gene exgA ( exg1 ) of Aspergillus oryzae Is Required to Catabolize Extracellular Glucan, and Is Induced in Growth on a Solid Surface Tamano, Koichi; Satoh, Yuki; Ishii, Tomoko Bioscience, Biotechnology, and Biochemistry, Vol. 71, Issue 4 https://doi.org/10.1271/bbb.60591	journal	April 2007
Transformation System for Aspergillus oryzae with Double Auxotrophic Mutations, niaD and sC Yamada, Osamu; Lee, Byung Rho; Gomi, Katsuya Bioscience, Biotechnology, and Biochemistry, Vol. 61, Issue 8 https://doi.org/10.1271/bbb.61.1367	journal	January 1997
Architecture and Functional Analysis of Fungal Polyketide Synthases Fujii, Isao; Watanabe, Akira; Tada, Hidenori Mycotoxins, Vol. 52, Issue 2 https://doi.org/10.2520/myco.52.135	journal	January 2002

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Alanine substitution in cellobiohydrolase provides new insights into substrate threading Mitsuzawa, Shigenobu; Fukuura, Maiko; Shinkawa, Satoru Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-16434-x	journal	November 2017
Aspergillus oryzae-based cell factory for direct kojic acid production from cellulose Yamada, Ryosuke; Yoshie, Toshihide; Wakai, Satoshi Microbial Cell Factories, Vol. 13, Issue 1 https://doi.org/10.1186/1475-2859-13-71	journal	May 2014
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Promoter tools for further development of Aspergillus oryzae as a platform for fungal secondary metabolite production Umemura, Maiko; Kuriiwa, Kaoru; Dao, Linh Viet Fungal Biology and Biotechnology, Vol. 7, Issue 1 https://doi.org/10.1186/s40694-020-00093-1	journal	March 2020

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59 BASIC BIOLOGICAL SCIENCES
Aspergillus oryzae
Ayg1-like hydrolase
Colony color
Conidial pigmentation
Filamentous fungi
Laccases

Major involvement of two laccase genes in conidial pigment biosynthesis in Aspergillus oryzae

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