Metabolic Responses of Carotenoid and Cordycepin Biosynthetic Pathways in <i>Cordyceps militaris</i> under Light-Programming Exposure through Genome-Wide Transcriptional Analysis

<i>Cordyceps militaris</i> is currently exploited for commercial production of specialty products as its biomass constituents are enriched in bioactive compounds, such as cordycepin. The rational process development is important for economically feasible production of high quality biopro...

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Main Authors: Roypim Thananusak, Kobkul Laoteng, Nachon Raethong, Yu Zhang, Wanwipa Vongsangnak
Format: Article
Language:English
Published: MDPI AG 2020-08-01
Series:Biology
Subjects:
Online Access:https://www.mdpi.com/2079-7737/9/9/242
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author Roypim Thananusak
Kobkul Laoteng
Nachon Raethong
Yu Zhang
Wanwipa Vongsangnak
author_facet Roypim Thananusak
Kobkul Laoteng
Nachon Raethong
Yu Zhang
Wanwipa Vongsangnak
author_sort Roypim Thananusak
collection DOAJ
description <i>Cordyceps militaris</i> is currently exploited for commercial production of specialty products as its biomass constituents are enriched in bioactive compounds, such as cordycepin. The rational process development is important for economically feasible production of high quality bioproducts. Light is an abiotic factor affecting the cultivation process of this entomopathogenic fungus, particularly in its carotenoid formation. To uncover the cell response to light exposure, this study aimed to systematically investigate the metabolic responses of <i>C. militaris</i> strain TBRC6039 using integrative genome-wide transcriptome and genome-scale metabolic network (GSMN)-driven analysis. The genome-wide transcriptome analysis showed 8747 expressed genes in the glucose and sucrose cultures grown under light-programming and dark conditions. Of them, 689 differentially expressed genes were significant in response to the light-programming exposure. Through integration with the GSMN-driven analysis using the improved network (<i>i</i>RT1467), the reporter metabolites, e.g., adenosine-5′-monophosphate (AMP) and 2-oxoglutarate, were identified when cultivated under the carotenoid-producing condition controlled by light-programming exposure, linking to up-regulations of the metabolic genes involved in glyoxalase system, as well as cordycepin and carotenoid biosynthesis. These results indicated that <i>C. militaris</i> had a metabolic control in acclimatization to light exposure through transcriptional co-regulation, which supported the cell growth and cordycepin production in addition to the accumulation of carotenoid as a photo-protective bio-pigment. This study provides a perspective in manipulating the metabolic fluxes towards the target metabolites through either genetic or physiological approaches.
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spelling doaj.art-f73c8e6674c041ff8b38383d6ec555c72023-11-20T10:54:28ZengMDPI AGBiology2079-77372020-08-019924210.3390/biology9090242Metabolic Responses of Carotenoid and Cordycepin Biosynthetic Pathways in <i>Cordyceps militaris</i> under Light-Programming Exposure through Genome-Wide Transcriptional AnalysisRoypim Thananusak0Kobkul Laoteng1Nachon Raethong2Yu Zhang3Wanwipa Vongsangnak4Interdisciplinary Graduate Program in Bioscience, Faculty of Science, Kasetsart University, Bangkok 10900, ThailandIndustrial Bioprocess Technology Research Team, Functional Ingredients and Food Innovation Research Group, National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Pathum Thani 12120, ThailandDepartment of Zoology, Faculty of Science, Kasetsart University, Bangkok 10900, ThailandKey Laboratory for Animal Genetics, Breeding, Reproduction and Molecular Design of Jiangsu Province, Yangzhou University, Yangzhou 225009, ChinaInterdisciplinary Graduate Program in Bioscience, Faculty of Science, Kasetsart University, Bangkok 10900, Thailand<i>Cordyceps militaris</i> is currently exploited for commercial production of specialty products as its biomass constituents are enriched in bioactive compounds, such as cordycepin. The rational process development is important for economically feasible production of high quality bioproducts. Light is an abiotic factor affecting the cultivation process of this entomopathogenic fungus, particularly in its carotenoid formation. To uncover the cell response to light exposure, this study aimed to systematically investigate the metabolic responses of <i>C. militaris</i> strain TBRC6039 using integrative genome-wide transcriptome and genome-scale metabolic network (GSMN)-driven analysis. The genome-wide transcriptome analysis showed 8747 expressed genes in the glucose and sucrose cultures grown under light-programming and dark conditions. Of them, 689 differentially expressed genes were significant in response to the light-programming exposure. Through integration with the GSMN-driven analysis using the improved network (<i>i</i>RT1467), the reporter metabolites, e.g., adenosine-5′-monophosphate (AMP) and 2-oxoglutarate, were identified when cultivated under the carotenoid-producing condition controlled by light-programming exposure, linking to up-regulations of the metabolic genes involved in glyoxalase system, as well as cordycepin and carotenoid biosynthesis. These results indicated that <i>C. militaris</i> had a metabolic control in acclimatization to light exposure through transcriptional co-regulation, which supported the cell growth and cordycepin production in addition to the accumulation of carotenoid as a photo-protective bio-pigment. This study provides a perspective in manipulating the metabolic fluxes towards the target metabolites through either genetic or physiological approaches.https://www.mdpi.com/2079-7737/9/9/242<i>Cordyceps militaris</i>carotenoidcordycepinlight responsetranscriptome analysisgenome-scale metabolic network
spellingShingle Roypim Thananusak
Kobkul Laoteng
Nachon Raethong
Yu Zhang
Wanwipa Vongsangnak
Metabolic Responses of Carotenoid and Cordycepin Biosynthetic Pathways in <i>Cordyceps militaris</i> under Light-Programming Exposure through Genome-Wide Transcriptional Analysis
Biology
<i>Cordyceps militaris</i>
carotenoid
cordycepin
light response
transcriptome analysis
genome-scale metabolic network
title Metabolic Responses of Carotenoid and Cordycepin Biosynthetic Pathways in <i>Cordyceps militaris</i> under Light-Programming Exposure through Genome-Wide Transcriptional Analysis
title_full Metabolic Responses of Carotenoid and Cordycepin Biosynthetic Pathways in <i>Cordyceps militaris</i> under Light-Programming Exposure through Genome-Wide Transcriptional Analysis
title_fullStr Metabolic Responses of Carotenoid and Cordycepin Biosynthetic Pathways in <i>Cordyceps militaris</i> under Light-Programming Exposure through Genome-Wide Transcriptional Analysis
title_full_unstemmed Metabolic Responses of Carotenoid and Cordycepin Biosynthetic Pathways in <i>Cordyceps militaris</i> under Light-Programming Exposure through Genome-Wide Transcriptional Analysis
title_short Metabolic Responses of Carotenoid and Cordycepin Biosynthetic Pathways in <i>Cordyceps militaris</i> under Light-Programming Exposure through Genome-Wide Transcriptional Analysis
title_sort metabolic responses of carotenoid and cordycepin biosynthetic pathways in i cordyceps militaris i under light programming exposure through genome wide transcriptional analysis
topic <i>Cordyceps militaris</i>
carotenoid
cordycepin
light response
transcriptome analysis
genome-scale metabolic network
url https://www.mdpi.com/2079-7737/9/9/242
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AT nachonraethong metabolicresponsesofcarotenoidandcordycepinbiosyntheticpathwaysinicordycepsmilitarisiunderlightprogrammingexposurethroughgenomewidetranscriptionalanalysis
AT yuzhang metabolicresponsesofcarotenoidandcordycepinbiosyntheticpathwaysinicordycepsmilitarisiunderlightprogrammingexposurethroughgenomewidetranscriptionalanalysis
AT wanwipavongsangnak metabolicresponsesofcarotenoidandcordycepinbiosyntheticpathwaysinicordycepsmilitarisiunderlightprogrammingexposurethroughgenomewidetranscriptionalanalysis