Genomic and Secretomic Analyses Reveal Unique Features of the Lignocellulolytic Enzyme System of Penicillium decumbens

Liu, Guodong; Zhang, Lei; Wei, Xiaomin; Zou, Gen; Qin, Yuqi; Ma, Liang; Li, Jie; Zheng, Huajun; Wang, Shengyue; Wang, Chengshu; Xun, Luying; Zhao, Guo-Ping; Zhou, Zhihua; Qu, Yinbo

doi:10.1371/journal.pone.0055185

Genomic and Secretomic Analyses Reveal Unique Features of the Lignocellulolytic Enzyme System of Penicillium decumbens

Journal Article · Fri Feb 01 00:00:00 EST 2013 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0055185· OSTI ID:1627583

Liu, Guodong ^[1]; Zhang, Lei ^[2]; Wei, Xiaomin ^[3]; Zou, Gen ^[2]; Qin, Yuqi ^[3]; Ma, Liang ^[2]; Li, Jie ^[3]; Zheng, Huajun ^[4]; Wang, Shengyue ^[4]; Wang, Chengshu ^[2]; Xun, Luying ^[5]; Zhao, Guo-Ping ^[6]; Zhou, Zhihua ^[2]; Qu, Yinbo ^[3]

Shandong University, Jinan (China); DOE/OSTI
Chinese Academy of Sciences (CAS), Shanghai (China)
Shandong University, Jinan (China)
Chinese National Human Genome Center at Shanghai (China)
Shandong University, Jinan (China); Washington State University, Pullman, WA (United States)
Chinese Academy of Sciences (CAS), Shanghai (China); Chinese National Human Genome Center at Shanghai (China)

Many Penicillium species could produce extracellular enzyme systems with good lignocellulose hydrolysis performance. However, these species and their enzyme systems are still poorly understood and explored due to the lacking of genetic information. Here, we present the genomic and secretomic analyses of Penicillium decumbens that has been used in industrial production of lignocellulolytic enzymes in China for more than fifteen years. Comparative genomics analysis with the phylogenetically most similar species Penicillium chrysogenum revealed that P. decumbens has evolved with more genes involved in plant cell wall degradation, but fewer genes in cellular metabolism and regulation. Compared with the widely used cellulase producer Trichoderma reesei, P. decumbens has a lignocellulolytic enzyme system with more diverse components, particularly for cellulose binding domain-containing proteins and hemicellulases. Further, proteomic analysis of secretomes revealed that P. decumbens produced significantly more lignocellulolytic enzymes in the medium with cellulose-wheat bran as the carbon source than with glucose. The results expand our knowledge on the genetic information of lignocellulolytic enzyme systems in Penicillium species, and will facilitate rational strain improvement for the production of highly efficient enzyme systems used in lignocellulose utilization from Penicillium species.

View Accepted Manuscript (DOE)

Research Organization:: Joint Genome Institute (JGI), Berkeley, CA (United States)

Sponsoring Organization:: Broad Institute of Harvard and MIT; International S&T Cooperation Program of China; National Basic Research Program of China; National Natural Sciences Foundation of China; USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1627583

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 2 Vol. 8; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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A review of bioreactor technology used for enzymatic hydrolysis of cellulosic materials Shokrkar, Hanieh; Ebrahimi, Sirous; Zamani, Mehdi Cellulose, Vol. 25, Issue 11 https://doi.org/10.1007/s10570-018-2028-4	journal	September 2018
Comparative Secretome Analysis of Aspergillus niger, Trichoderma reesei, and Penicillium oxalicum During Solid-State Fermentation Gong, Weili; Zhang, Huaiqiang; Liu, Shijia Applied Biochemistry and Biotechnology, Vol. 177, Issue 6 https://doi.org/10.1007/s12010-015-1811-z	journal	August 2015
Efficient genome editing in filamentous fungus Trichoderma reesei using the CRISPR/Cas9 system Liu, Rui; Chen, Ling; Jiang, Yanping Cell Discovery, Vol. 1, Article No. 15007 https://doi.org/10.1038/celldisc.2015.7	journal	May 2015
Functional diversity and properties of multiple xylanases from Penicillium oxalicum GZ-2 Liao, Hanpeng; Zheng, Haiping; Li, Shuixian Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep12631	journal	July 2015
Structure revision of cryptosporioptides and determination of the genetic basis for dimeric xanthone biosynthesis in fungi Greco, Claudio; de Mattos-Shipley, Kate; Bailey, Andrew M. Chemical Science, Vol. 10, Issue 10 https://doi.org/10.1039/c8sc05126g	journal	January 2019
Horizontal gene transfer and gene dosage drives adaptation to wood colonization in a tree pathogen Dhillon, Braham; Feau, Nicolas; Aerts, Andrea L. Proceedings of the National Academy of Sciences, Vol. 112, Issue 11 https://doi.org/10.1073/pnas.1424293112	journal	March 2015
Deletion of the middle region of the transcription factor ClrB in Penicillium oxalicum enables cellulase production in the presence of glucose Gao, Liwei; Xu, Yanning; Song, Xin Journal of Biological Chemistry, Vol. 294, Issue 49 https://doi.org/10.1074/jbc.ra119.010863	journal	October 2019
A Novel Cys2His2 Zinc Finger Homolog of AZF1 Modulates Holocellulase Expression in Trichoderma reesei Antonieto, Amanda Cristina Campos; Nogueira, Karoline Maria Vieira; de Paula, Renato Graciano mSystems, Vol. 4, Issue 4 https://doi.org/10.1128/msystems.00161-19	journal	August 2019
Insights into high-efficiency lignocellulolytic enzyme production by Penicillium oxalicum GZ-2 induced by a complex substrate Liao, Hanpeng; Li, Shuixian; Wei, Zhong Biotechnology for Biofuels, Vol. 7, Issue 1 https://doi.org/10.1186/s13068-014-0162-2	journal	November 2014
Penicillium echinulatum secretome analysis reveals the fungi potential for degradation of lignocellulosic biomass Schneider, Willian Daniel Hahn; Gonçalves, Thiago Augusto; Uchima, Cristiane Akemi Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0476-3	journal	March 2016
Proteomic analysis of the biomass hydrolytic potentials of Penicillium oxalicum lignocellulolytic enzyme system Song, Wenxia; Han, Xiaolong; Qian, Yuanchao Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0477-2	journal	March 2016
Production of a high-efficiency cellulase complex via β-glucosidase engineering in Penicillium oxalicum Yao, Guangshan; Wu, Ruimei; Kan, Qinbiao Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0491-4	journal	March 2016
Adsorption and mechanism of cellulase enzymes onto lignin isolated from corn stover pretreated with liquid hot water Lu, Xianqin; Zheng, Xiaoju; Li, Xuezhi Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0531-0	journal	June 2016
Comparative genomic, transcriptomic and secretomic profiling of Penicillium oxalicum HP7-1 and its cellulase and xylanase hyper-producing mutant EU2106, and identification of two novel regulatory genes of cellulase and xylanase gene expression Zhao, Shuai; Yan, Yu-Si; He, Qi-Peng Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0616-9	journal	September 2016
Expression and chromatin structures of cellulolytic enzyme gene regulated by heterochromatin protein 1 Zhang, Xiujun; Qu, Yinbo; Qin, Yuqi Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0624-9	journal	October 2016
Combining manipulation of transcription factors and overexpression of the target genes to enhance lignocellulolytic enzyme production in Penicillium oxalicum Gao, Liwei; Li, Zhonghai; Xia, Chengqiang Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0783-3	journal	April 2017
The putative β-glucosidase BGL3I regulates cellulase induction in Trichoderma reesei Zou, Gen; Jiang, Yanping; Liu, Rui Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1314-6	journal	November 2018
Normal transcription of cellulolytic enzyme genes relies on the balance between the methylation of H3K36 and H3K4 in Penicillium oxalicum Li, Yanan; Hu, Yueyan; Zhu, Zhu Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1539-z	journal	August 2019
Cloning and expression of a novel α-1,3-arabinofuranosidase from Penicillium oxalicum sp. 68 Hu, Yanbo; Yan, Xuecui; Zhang, Han AMB Express, Vol. 8, Issue 1 https://doi.org/10.1186/s13568-018-0577-4	journal	April 2018
Synergistic and Dose-Controlled Regulation of Cellulase Gene Expression in Penicillium oxalicum Li, Zhonghai; Yao, Guangshan; Wu, Ruimei PLOS Genetics, Vol. 11, Issue 9 https://doi.org/10.1371/journal.pgen.1005509	journal	September 2015
The Different Roles of Penicillium oxalicum LaeA in the Production of Extracellular Cellulase and β-xylosidase Li, Yanan; Zheng, Xiaoju; Zhang, Xiujun Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.02091	journal	December 2016
The Indispensable Role of Histone Methyltransferase PoDot1 in Extracellular Glycoside Hydrolase Biosynthesis of Penicillium oxalicum Li, Yanan; Hu, Yueyan; Zhao, Kaili Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02566	journal	November 2019
Engineering Robust Cellulases for Tailored Lignocellulosic Degradation Cocktails Contreras, Francisca; Pramanik, Subrata; M. Rozhkova, Aleksandra International Journal of Molecular Sciences, Vol. 21, Issue 5 https://doi.org/10.3390/ijms21051589	journal	February 2020

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