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Cysteine facilitates the lignocellulolytic response of Trichoderma guizhouense NJAU4742 by indirectly up-regulating membrane sugar transporters

BACKGROUND: Filamentous fungi possess a rich CAZymes system, which is widely studied and applied in the bio-conversion of plant biomass to alcohol chemicals. Carbon source acquisition is the fundamental driver for CAZymes-producing sustainability and secondary metabolism, therefore, a deeper insight...

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Autores principales: Liu, Yang, Li, Tuo, Zhu, Han, Zhou, Yihao, Shen, Qirong, Liu, Dongyang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10612256/
https://www.ncbi.nlm.nih.gov/pubmed/37891614
http://dx.doi.org/10.1186/s13068-023-02418-9
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author Liu, Yang
Li, Tuo
Zhu, Han
Zhou, Yihao
Shen, Qirong
Liu, Dongyang
author_facet Liu, Yang
Li, Tuo
Zhu, Han
Zhou, Yihao
Shen, Qirong
Liu, Dongyang
author_sort Liu, Yang
collection PubMed
description BACKGROUND: Filamentous fungi possess a rich CAZymes system, which is widely studied and applied in the bio-conversion of plant biomass to alcohol chemicals. Carbon source acquisition is the fundamental driver for CAZymes-producing sustainability and secondary metabolism, therefore, a deeper insight into the regulatory network of sugar transport in filamentous fungi has become urgent. RESULTS: This study reports an important linkage of sulfur assimilation to lignocellulose response of filamentous fungus. Inorganic sulfur addition facilitated biodegradation of rice straw by Trichoderma guizhouense NJAU4742. Cysteine and glutathione were revealed as major intracellular metabolites responsive to sulfur addition by metabolomics, cysteine content was increased in this process and glutathione increased correspondingly. Two membrane sugar transporter genes, Tgmst1 and Tgmst2, were identified as the critical response genes significantly up-regulated when intracellular cysteine increased. Tgmst1 and Tgmst2 were both positively regulated by the glucose regulation-related protein (GRP), up-regulation of both Tgmst1 and Tggrp can cause a significant increase in intracellular glucose. The transcriptional regulatory function of GRP mainly relied on GSH-induced glutathionylation, and the transcription activating efficiency was positively related to the glutathionylation level, furthermore, DTT-induced deglutathionylation resulted in the down-regulation of downstream genes. CONCLUSIONS: Inorganic sulfur addition induces a rise in intracellular Cys content, and the conversion of cysteine to glutathione caused the increase of glutathionylation level of GRP, which in turn up-regulated Tgmst1 and Tgmst2. Subsequently, the sugar transport efficiency of single cells was improved, which facilitated the maintenance of vigorous CAZymes metabolism and the straw-to-biomass conversion. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13068-023-02418-9.
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spelling pubmed-106122562023-10-29 Cysteine facilitates the lignocellulolytic response of Trichoderma guizhouense NJAU4742 by indirectly up-regulating membrane sugar transporters Liu, Yang Li, Tuo Zhu, Han Zhou, Yihao Shen, Qirong Liu, Dongyang Biotechnol Biofuels Bioprod Research BACKGROUND: Filamentous fungi possess a rich CAZymes system, which is widely studied and applied in the bio-conversion of plant biomass to alcohol chemicals. Carbon source acquisition is the fundamental driver for CAZymes-producing sustainability and secondary metabolism, therefore, a deeper insight into the regulatory network of sugar transport in filamentous fungi has become urgent. RESULTS: This study reports an important linkage of sulfur assimilation to lignocellulose response of filamentous fungus. Inorganic sulfur addition facilitated biodegradation of rice straw by Trichoderma guizhouense NJAU4742. Cysteine and glutathione were revealed as major intracellular metabolites responsive to sulfur addition by metabolomics, cysteine content was increased in this process and glutathione increased correspondingly. Two membrane sugar transporter genes, Tgmst1 and Tgmst2, were identified as the critical response genes significantly up-regulated when intracellular cysteine increased. Tgmst1 and Tgmst2 were both positively regulated by the glucose regulation-related protein (GRP), up-regulation of both Tgmst1 and Tggrp can cause a significant increase in intracellular glucose. The transcriptional regulatory function of GRP mainly relied on GSH-induced glutathionylation, and the transcription activating efficiency was positively related to the glutathionylation level, furthermore, DTT-induced deglutathionylation resulted in the down-regulation of downstream genes. CONCLUSIONS: Inorganic sulfur addition induces a rise in intracellular Cys content, and the conversion of cysteine to glutathione caused the increase of glutathionylation level of GRP, which in turn up-regulated Tgmst1 and Tgmst2. Subsequently, the sugar transport efficiency of single cells was improved, which facilitated the maintenance of vigorous CAZymes metabolism and the straw-to-biomass conversion. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13068-023-02418-9. BioMed Central 2023-10-27 /pmc/articles/PMC10612256/ /pubmed/37891614 http://dx.doi.org/10.1186/s13068-023-02418-9 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Liu, Yang
Li, Tuo
Zhu, Han
Zhou, Yihao
Shen, Qirong
Liu, Dongyang
Cysteine facilitates the lignocellulolytic response of Trichoderma guizhouense NJAU4742 by indirectly up-regulating membrane sugar transporters
title Cysteine facilitates the lignocellulolytic response of Trichoderma guizhouense NJAU4742 by indirectly up-regulating membrane sugar transporters
title_full Cysteine facilitates the lignocellulolytic response of Trichoderma guizhouense NJAU4742 by indirectly up-regulating membrane sugar transporters
title_fullStr Cysteine facilitates the lignocellulolytic response of Trichoderma guizhouense NJAU4742 by indirectly up-regulating membrane sugar transporters
title_full_unstemmed Cysteine facilitates the lignocellulolytic response of Trichoderma guizhouense NJAU4742 by indirectly up-regulating membrane sugar transporters
title_short Cysteine facilitates the lignocellulolytic response of Trichoderma guizhouense NJAU4742 by indirectly up-regulating membrane sugar transporters
title_sort cysteine facilitates the lignocellulolytic response of trichoderma guizhouense njau4742 by indirectly up-regulating membrane sugar transporters
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10612256/
https://www.ncbi.nlm.nih.gov/pubmed/37891614
http://dx.doi.org/10.1186/s13068-023-02418-9
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