The transcriptional factor Clr-5 is involved in cellulose degradation through regulation of amino acid metabolism in Neurospora crassa
Abstract Background Filamentous fungi are efficient degraders of plant biomass and the primary producers of commercial cellulolytic enzymes. While the transcriptional regulation mechanisms of cellulases have been continuously explored in lignocellulolytic fungi, the induction of cellulase production...
Main Authors: | , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
BMC
2023-11-01
|
Series: | BMC Biotechnology |
Subjects: | |
Online Access: | https://doi.org/10.1186/s12896-023-00823-4 |
_version_ | 1797414759477280768 |
---|---|
author | Fanglei Xue Zhen Zhao Shuying Gu Meixin Chen Jing Xu Xuegang Luo Jingen Li Chaoguang Tian |
author_facet | Fanglei Xue Zhen Zhao Shuying Gu Meixin Chen Jing Xu Xuegang Luo Jingen Li Chaoguang Tian |
author_sort | Fanglei Xue |
collection | DOAJ |
description | Abstract Background Filamentous fungi are efficient degraders of plant biomass and the primary producers of commercial cellulolytic enzymes. While the transcriptional regulation mechanisms of cellulases have been continuously explored in lignocellulolytic fungi, the induction of cellulase production remains a complex multifactorial system, with several aspects still largely elusive. Results In this study, we identified a Zn2Cys6 transcription factor, designated as Clr-5, which regulates the expression of cellulase genes by influencing amino acid metabolism in Neurospora crassa during growth on cellulose. The deletion of clr-5 caused a significant decrease in secreted protein and cellulolytic enzyme activity of N. crassa, which was partially alleviated by supplementing with yeast extract. Transcriptomic profiling revealed downregulation of not only the genes encoding main cellulases but also those related to nitrogen metabolism after disruption of Clr-5 under Avicel condition. Clr-5 played a crucial role in the utilization of multiple amino acids, especially leucine and histidine. When using leucine or histidine as the sole nitrogen source, the Δclr-5 mutant showed significant growth defects on both glucose and Avicel media. Comparative transcriptomic analysis revealed that the transcript levels of most genes encoding carbohydrate-active enzymes and those involved in the catabolism and uptake of histidine, branched-chain amino acids, and aromatic amino acids, were remarkably reduced in strain Δclr-5, compared with the wild-type N. crassa when grown in Avicel medium with leucine or histidine as the sole nitrogen source. These findings underscore the important role of amino acid metabolism in the regulation of cellulase production in N. crassa. Furthermore, the function of Clr-5 in regulating cellulose degradation is conserved among ascomycete fungi. Conclusions These findings regarding the novel transcription factor Clr-5 enhance our comprehension of the regulatory connections between amino acid metabolism and cellulase production, offering fresh prospects for the development of fungal cell factories dedicated to cellulolytic enzyme production in bio-refineries. |
first_indexed | 2024-03-09T05:38:29Z |
format | Article |
id | doaj.art-e49586f15e91484badc0b6bfdf72b846 |
institution | Directory Open Access Journal |
issn | 1472-6750 |
language | English |
last_indexed | 2024-03-09T05:38:29Z |
publishDate | 2023-11-01 |
publisher | BMC |
record_format | Article |
series | BMC Biotechnology |
spelling | doaj.art-e49586f15e91484badc0b6bfdf72b8462023-12-03T12:27:08ZengBMCBMC Biotechnology1472-67502023-11-0123111410.1186/s12896-023-00823-4The transcriptional factor Clr-5 is involved in cellulose degradation through regulation of amino acid metabolism in Neurospora crassaFanglei Xue0Zhen Zhao1Shuying Gu2Meixin Chen3Jing Xu4Xuegang Luo5Jingen Li6Chaoguang Tian7College of Biotechnology, Tianjin University of Science and TechnologyKey Laboratory of Engineering Biology for Low-Carbon Manufacturing, Tianjin Institute of Industrial Biotechnology, Chinese Academy of SciencesKey Laboratory of Engineering Biology for Low-Carbon Manufacturing, Tianjin Institute of Industrial Biotechnology, Chinese Academy of SciencesCollege of Biotechnology, Tianjin University of Science and TechnologyKey Laboratory of Engineering Biology for Low-Carbon Manufacturing, Tianjin Institute of Industrial Biotechnology, Chinese Academy of SciencesCollege of Biotechnology, Tianjin University of Science and TechnologyKey Laboratory of Engineering Biology for Low-Carbon Manufacturing, Tianjin Institute of Industrial Biotechnology, Chinese Academy of SciencesKey Laboratory of Engineering Biology for Low-Carbon Manufacturing, Tianjin Institute of Industrial Biotechnology, Chinese Academy of SciencesAbstract Background Filamentous fungi are efficient degraders of plant biomass and the primary producers of commercial cellulolytic enzymes. While the transcriptional regulation mechanisms of cellulases have been continuously explored in lignocellulolytic fungi, the induction of cellulase production remains a complex multifactorial system, with several aspects still largely elusive. Results In this study, we identified a Zn2Cys6 transcription factor, designated as Clr-5, which regulates the expression of cellulase genes by influencing amino acid metabolism in Neurospora crassa during growth on cellulose. The deletion of clr-5 caused a significant decrease in secreted protein and cellulolytic enzyme activity of N. crassa, which was partially alleviated by supplementing with yeast extract. Transcriptomic profiling revealed downregulation of not only the genes encoding main cellulases but also those related to nitrogen metabolism after disruption of Clr-5 under Avicel condition. Clr-5 played a crucial role in the utilization of multiple amino acids, especially leucine and histidine. When using leucine or histidine as the sole nitrogen source, the Δclr-5 mutant showed significant growth defects on both glucose and Avicel media. Comparative transcriptomic analysis revealed that the transcript levels of most genes encoding carbohydrate-active enzymes and those involved in the catabolism and uptake of histidine, branched-chain amino acids, and aromatic amino acids, were remarkably reduced in strain Δclr-5, compared with the wild-type N. crassa when grown in Avicel medium with leucine or histidine as the sole nitrogen source. These findings underscore the important role of amino acid metabolism in the regulation of cellulase production in N. crassa. Furthermore, the function of Clr-5 in regulating cellulose degradation is conserved among ascomycete fungi. Conclusions These findings regarding the novel transcription factor Clr-5 enhance our comprehension of the regulatory connections between amino acid metabolism and cellulase production, offering fresh prospects for the development of fungal cell factories dedicated to cellulolytic enzyme production in bio-refineries.https://doi.org/10.1186/s12896-023-00823-4Neurospora crassaTranscription factorCellulase productionAmino acid metabolismClr-5 |
spellingShingle | Fanglei Xue Zhen Zhao Shuying Gu Meixin Chen Jing Xu Xuegang Luo Jingen Li Chaoguang Tian The transcriptional factor Clr-5 is involved in cellulose degradation through regulation of amino acid metabolism in Neurospora crassa BMC Biotechnology Neurospora crassa Transcription factor Cellulase production Amino acid metabolism Clr-5 |
title | The transcriptional factor Clr-5 is involved in cellulose degradation through regulation of amino acid metabolism in Neurospora crassa |
title_full | The transcriptional factor Clr-5 is involved in cellulose degradation through regulation of amino acid metabolism in Neurospora crassa |
title_fullStr | The transcriptional factor Clr-5 is involved in cellulose degradation through regulation of amino acid metabolism in Neurospora crassa |
title_full_unstemmed | The transcriptional factor Clr-5 is involved in cellulose degradation through regulation of amino acid metabolism in Neurospora crassa |
title_short | The transcriptional factor Clr-5 is involved in cellulose degradation through regulation of amino acid metabolism in Neurospora crassa |
title_sort | transcriptional factor clr 5 is involved in cellulose degradation through regulation of amino acid metabolism in neurospora crassa |
topic | Neurospora crassa Transcription factor Cellulase production Amino acid metabolism Clr-5 |
url | https://doi.org/10.1186/s12896-023-00823-4 |
work_keys_str_mv | AT fangleixue thetranscriptionalfactorclr5isinvolvedincellulosedegradationthroughregulationofaminoacidmetabolisminneurosporacrassa AT zhenzhao thetranscriptionalfactorclr5isinvolvedincellulosedegradationthroughregulationofaminoacidmetabolisminneurosporacrassa AT shuyinggu thetranscriptionalfactorclr5isinvolvedincellulosedegradationthroughregulationofaminoacidmetabolisminneurosporacrassa AT meixinchen thetranscriptionalfactorclr5isinvolvedincellulosedegradationthroughregulationofaminoacidmetabolisminneurosporacrassa AT jingxu thetranscriptionalfactorclr5isinvolvedincellulosedegradationthroughregulationofaminoacidmetabolisminneurosporacrassa AT xuegangluo thetranscriptionalfactorclr5isinvolvedincellulosedegradationthroughregulationofaminoacidmetabolisminneurosporacrassa AT jingenli thetranscriptionalfactorclr5isinvolvedincellulosedegradationthroughregulationofaminoacidmetabolisminneurosporacrassa AT chaoguangtian thetranscriptionalfactorclr5isinvolvedincellulosedegradationthroughregulationofaminoacidmetabolisminneurosporacrassa AT fangleixue transcriptionalfactorclr5isinvolvedincellulosedegradationthroughregulationofaminoacidmetabolisminneurosporacrassa AT zhenzhao transcriptionalfactorclr5isinvolvedincellulosedegradationthroughregulationofaminoacidmetabolisminneurosporacrassa AT shuyinggu transcriptionalfactorclr5isinvolvedincellulosedegradationthroughregulationofaminoacidmetabolisminneurosporacrassa AT meixinchen transcriptionalfactorclr5isinvolvedincellulosedegradationthroughregulationofaminoacidmetabolisminneurosporacrassa AT jingxu transcriptionalfactorclr5isinvolvedincellulosedegradationthroughregulationofaminoacidmetabolisminneurosporacrassa AT xuegangluo transcriptionalfactorclr5isinvolvedincellulosedegradationthroughregulationofaminoacidmetabolisminneurosporacrassa AT jingenli transcriptionalfactorclr5isinvolvedincellulosedegradationthroughregulationofaminoacidmetabolisminneurosporacrassa AT chaoguangtian transcriptionalfactorclr5isinvolvedincellulosedegradationthroughregulationofaminoacidmetabolisminneurosporacrassa |