Glutamine involvement in nitrogen regulation of cellulase production in fungi

Abstract Background Cellulase synthesized by fungi can environment-friendly and sustainably degrades cellulose to fermentable sugars for producing cellulosic biofuels, biobased medicine and fine chemicals. Great efforts have been made to study the regulation mechanism of cellulase biosynthesis in fu...

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Main Authors: Ai-Ping Pang, Funing Zhang, Xin Hu, Yongsheng Luo, Haiyan Wang, Samran Durrani, Fu-Gen Wu, Bing-Zhi Li, Zhihua Zhou, Zuhong Lu, Fengming Lin
Format: Article
Language:English
Published: BMC 2021-10-01
Series:Biotechnology for Biofuels
Subjects:
Online Access:https://doi.org/10.1186/s13068-021-02046-1
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author Ai-Ping Pang
Funing Zhang
Xin Hu
Yongsheng Luo
Haiyan Wang
Samran Durrani
Fu-Gen Wu
Bing-Zhi Li
Zhihua Zhou
Zuhong Lu
Fengming Lin
author_facet Ai-Ping Pang
Funing Zhang
Xin Hu
Yongsheng Luo
Haiyan Wang
Samran Durrani
Fu-Gen Wu
Bing-Zhi Li
Zhihua Zhou
Zuhong Lu
Fengming Lin
author_sort Ai-Ping Pang
collection DOAJ
description Abstract Background Cellulase synthesized by fungi can environment-friendly and sustainably degrades cellulose to fermentable sugars for producing cellulosic biofuels, biobased medicine and fine chemicals. Great efforts have been made to study the regulation mechanism of cellulase biosynthesis in fungi with the focus on the carbon sources, while little attention has been paid to the impact and regulation mechanism of nitrogen sources on cellulase production. Results Glutamine displayed the strongest inhibition effect on cellulase biosynthesis in Trichoderma reesei, followed by yeast extract, urea, tryptone, ammonium sulfate and l-glutamate. Cellulase production, cell growth and sporulation in T. reesei RUT-C30 grown on cellulose were all inhibited with the addition of glutamine (a preferred nitrogen source) with no change for mycelium morphology. This inhibition effect was attributed to both l-glutamine itself and the nitrogen excess induced by its presence. In agreement with the reduced cellulase production, the mRNA levels of 44 genes related to the cellulase production were decreased severely in the presence of glutamine. The transcriptional levels of genes involved in other nitrogen transport, ribosomal biogenesis and glutamine biosynthesis were decreased notably by glutamine, while the expression of genes relevant to glutamate biosynthesis, amino acid catabolism, and glutamine catabolism were increased noticeably. Moreover, the transcriptional level of cellulose signaling related proteins ooc1 and ooc2, and the cellular receptor of rapamycin trFKBP12 was increased remarkably, whose deletion exacerbated the cellulase depression influence of glutamine. Conclusion Glutamine may well be the metabolite effector in nitrogen repression of cellulase synthesis, like the role of glucose plays in carbon catabolite repression. Glutamine under excess nitrogen condition repressed cellulase biosynthesis significantly as well as cell growth and sporulation in T. reesei RUT-C30. More importantly, the presence of glutamine notably impacted the transport and metabolism of nitrogen. Genes ooc1, ooc2, and trFKBP12 are associated with the cellulase repression impact of glutamine. These findings advance our understanding of nitrogen regulation of cellulase production in filamentous fungi, which would aid in the rational design of strains and fermentation strategies for cellulase production in industry.
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spelling doaj.art-a30fbab3e79b422eb6ca6bee039e73b42022-12-22T03:36:22ZengBMCBiotechnology for Biofuels1754-68342021-10-0114111610.1186/s13068-021-02046-1Glutamine involvement in nitrogen regulation of cellulase production in fungiAi-Ping Pang0Funing Zhang1Xin Hu2Yongsheng Luo3Haiyan Wang4Samran Durrani5Fu-Gen Wu6Bing-Zhi Li7Zhihua Zhou8Zuhong Lu9Fengming Lin10State Key Laboratory of Bioelectronics, School of Biological Science and Medical Engineering, Southeast UniversityState Key Laboratory of Bioelectronics, School of Biological Science and Medical Engineering, Southeast UniversityState Key Laboratory of Bioelectronics, School of Biological Science and Medical Engineering, Southeast UniversityState Key Laboratory of Bioelectronics, School of Biological Science and Medical Engineering, Southeast UniversityState Key Laboratory of Bioelectronics, School of Biological Science and Medical Engineering, Southeast UniversityState Key Laboratory of Bioelectronics, School of Biological Science and Medical Engineering, Southeast UniversityState Key Laboratory of Bioelectronics, School of Biological Science and Medical Engineering, Southeast UniversityKey Laboratory of Systems Bioengineering (Ministry of Education), School of Chemical Engineering and Technology, Tianjin UniversityKey Laboratory of Synthetic Biology, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of SciencesState Key Laboratory of Bioelectronics, School of Biological Science and Medical Engineering, Southeast UniversityState Key Laboratory of Bioelectronics, School of Biological Science and Medical Engineering, Southeast UniversityAbstract Background Cellulase synthesized by fungi can environment-friendly and sustainably degrades cellulose to fermentable sugars for producing cellulosic biofuels, biobased medicine and fine chemicals. Great efforts have been made to study the regulation mechanism of cellulase biosynthesis in fungi with the focus on the carbon sources, while little attention has been paid to the impact and regulation mechanism of nitrogen sources on cellulase production. Results Glutamine displayed the strongest inhibition effect on cellulase biosynthesis in Trichoderma reesei, followed by yeast extract, urea, tryptone, ammonium sulfate and l-glutamate. Cellulase production, cell growth and sporulation in T. reesei RUT-C30 grown on cellulose were all inhibited with the addition of glutamine (a preferred nitrogen source) with no change for mycelium morphology. This inhibition effect was attributed to both l-glutamine itself and the nitrogen excess induced by its presence. In agreement with the reduced cellulase production, the mRNA levels of 44 genes related to the cellulase production were decreased severely in the presence of glutamine. The transcriptional levels of genes involved in other nitrogen transport, ribosomal biogenesis and glutamine biosynthesis were decreased notably by glutamine, while the expression of genes relevant to glutamate biosynthesis, amino acid catabolism, and glutamine catabolism were increased noticeably. Moreover, the transcriptional level of cellulose signaling related proteins ooc1 and ooc2, and the cellular receptor of rapamycin trFKBP12 was increased remarkably, whose deletion exacerbated the cellulase depression influence of glutamine. Conclusion Glutamine may well be the metabolite effector in nitrogen repression of cellulase synthesis, like the role of glucose plays in carbon catabolite repression. Glutamine under excess nitrogen condition repressed cellulase biosynthesis significantly as well as cell growth and sporulation in T. reesei RUT-C30. More importantly, the presence of glutamine notably impacted the transport and metabolism of nitrogen. Genes ooc1, ooc2, and trFKBP12 are associated with the cellulase repression impact of glutamine. These findings advance our understanding of nitrogen regulation of cellulase production in filamentous fungi, which would aid in the rational design of strains and fermentation strategies for cellulase production in industry.https://doi.org/10.1186/s13068-021-02046-1GlutamineCellulaseNitrogen metabolismThe TOR pathwayooc1trFKBP12
spellingShingle Ai-Ping Pang
Funing Zhang
Xin Hu
Yongsheng Luo
Haiyan Wang
Samran Durrani
Fu-Gen Wu
Bing-Zhi Li
Zhihua Zhou
Zuhong Lu
Fengming Lin
Glutamine involvement in nitrogen regulation of cellulase production in fungi
Biotechnology for Biofuels
Glutamine
Cellulase
Nitrogen metabolism
The TOR pathway
ooc1
trFKBP12
title Glutamine involvement in nitrogen regulation of cellulase production in fungi
title_full Glutamine involvement in nitrogen regulation of cellulase production in fungi
title_fullStr Glutamine involvement in nitrogen regulation of cellulase production in fungi
title_full_unstemmed Glutamine involvement in nitrogen regulation of cellulase production in fungi
title_short Glutamine involvement in nitrogen regulation of cellulase production in fungi
title_sort glutamine involvement in nitrogen regulation of cellulase production in fungi
topic Glutamine
Cellulase
Nitrogen metabolism
The TOR pathway
ooc1
trFKBP12
url https://doi.org/10.1186/s13068-021-02046-1
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