Disruption of the Ergosterol Biosynthetic Pathway Results in Increased Membrane Permeability, Causing Overproduction and Secretion of Extracellular Monascus Pigments in Submerged Fermentation
Because Monascus pigments (MPs) predominantly accumulate in the cytoplasm during submerged fermentation, many biotechnologies are applied to enhance the production of extracellular MPs (exMPs) to reduce the downstream processing costs. In this study, the genes monascus_7017 and monascus_8018, identi...
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| Veröffentlicht in: | Journal of agricultural and food chemistry 2019-12, Vol.67 (49), p.13673-13683 |
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| container_title | Journal of agricultural and food chemistry |
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| creator | Liu, Jun Chai, Xueying Guo, Ting Wu, Jingyan Yang, Pengpeng Luo, Yunchuan Zhao, Hui Zhao, Wen Nkechi, Omeoga Dong, Jie Bai, Jie Lin, Qinlu |
| description | Because Monascus pigments (MPs) predominantly accumulate in the cytoplasm during submerged fermentation, many biotechnologies are applied to enhance the production of extracellular MPs (exMPs) to reduce the downstream processing costs. In this study, the genes monascus_7017 and monascus_8018, identified as ERG4 genes, were knocked out to disrupt the ergosterol biosynthetic pathway and enhance the production of exMPs in Monascus purpureus LQ-6. Double-deletion of EGR4 in M. purpureus LQ-6 reduced ergosterol concentration by 57.14% and enhanced exMP production 2.06-fold. In addition, integrated transcriptomic and proteomic analyses were performed to elucidate the transmembrane secretion mechanism of exMPs based on the relationship between ergosterol synthesis and membrane permeability, which revealed that several metabolic pathways were noticeably dynamic, including fatty acid degradation, amino acid metabolism, energy metabolism, carbohydrate metabolism, and transport. These findings therefore clarified the secretion mechanism of exMPs and provide a novel strategy for further enhancement of exMP production in submerged fermentation. |
| doi_str_mv | 10.1021/acs.jafc.9b05872 |
| format | Article |
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In this study, the genes monascus_7017 and monascus_8018, identified as ERG4 genes, were knocked out to disrupt the ergosterol biosynthetic pathway and enhance the production of exMPs in Monascus purpureus LQ-6. Double-deletion of EGR4 in M. purpureus LQ-6 reduced ergosterol concentration by 57.14% and enhanced exMP production 2.06-fold. In addition, integrated transcriptomic and proteomic analyses were performed to elucidate the transmembrane secretion mechanism of exMPs based on the relationship between ergosterol synthesis and membrane permeability, which revealed that several metabolic pathways were noticeably dynamic, including fatty acid degradation, amino acid metabolism, energy metabolism, carbohydrate metabolism, and transport. These findings therefore clarified the secretion mechanism of exMPs and provide a novel strategy for further enhancement of exMP production in submerged fermentation.</description><identifier>ISSN: 0021-8561</identifier><identifier>EISSN: 1520-5118</identifier><identifier>DOI: 10.1021/acs.jafc.9b05872</identifier><identifier>PMID: 31617717</identifier><language>eng</language><publisher>United States: American Chemical Society</publisher><subject>Biosynthetic Pathways ; Cell Membrane - genetics ; Cell Membrane - metabolism ; Cell Membrane Permeability ; Ergosterol - biosynthesis ; Fermentation ; Fungal Proteins - genetics ; Fungal Proteins - metabolism ; Monascus - genetics ; Monascus - metabolism ; Pigments, Biological - biosynthesis</subject><ispartof>Journal of agricultural and food chemistry, 2019-12, Vol.67 (49), p.13673-13683</ispartof><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-a336t-413ad457f943be222c7c52fc329a0b16be9b3db26367238d6b274baceb32c9673</citedby><cites>FETCH-LOGICAL-a336t-413ad457f943be222c7c52fc329a0b16be9b3db26367238d6b274baceb32c9673</cites><orcidid>0000-0002-5322-3916</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://pubs.acs.org/doi/pdf/10.1021/acs.jafc.9b05872$$EPDF$$P50$$Gacs$$H</linktopdf><linktohtml>$$Uhttps://pubs.acs.org/doi/10.1021/acs.jafc.9b05872$$EHTML$$P50$$Gacs$$H</linktohtml><link.rule.ids>314,780,784,2763,27075,27923,27924,56737,56787</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31617717$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Liu, Jun</creatorcontrib><creatorcontrib>Chai, Xueying</creatorcontrib><creatorcontrib>Guo, Ting</creatorcontrib><creatorcontrib>Wu, Jingyan</creatorcontrib><creatorcontrib>Yang, Pengpeng</creatorcontrib><creatorcontrib>Luo, Yunchuan</creatorcontrib><creatorcontrib>Zhao, Hui</creatorcontrib><creatorcontrib>Zhao, Wen</creatorcontrib><creatorcontrib>Nkechi, Omeoga</creatorcontrib><creatorcontrib>Dong, Jie</creatorcontrib><creatorcontrib>Bai, Jie</creatorcontrib><creatorcontrib>Lin, Qinlu</creatorcontrib><title>Disruption of the Ergosterol Biosynthetic Pathway Results in Increased Membrane Permeability, Causing Overproduction and Secretion of Extracellular Monascus Pigments in Submerged Fermentation</title><title>Journal of agricultural and food chemistry</title><addtitle>J. Agric. Food Chem</addtitle><description>Because Monascus pigments (MPs) predominantly accumulate in the cytoplasm during submerged fermentation, many biotechnologies are applied to enhance the production of extracellular MPs (exMPs) to reduce the downstream processing costs. In this study, the genes monascus_7017 and monascus_8018, identified as ERG4 genes, were knocked out to disrupt the ergosterol biosynthetic pathway and enhance the production of exMPs in Monascus purpureus LQ-6. Double-deletion of EGR4 in M. purpureus LQ-6 reduced ergosterol concentration by 57.14% and enhanced exMP production 2.06-fold. In addition, integrated transcriptomic and proteomic analyses were performed to elucidate the transmembrane secretion mechanism of exMPs based on the relationship between ergosterol synthesis and membrane permeability, which revealed that several metabolic pathways were noticeably dynamic, including fatty acid degradation, amino acid metabolism, energy metabolism, carbohydrate metabolism, and transport. These findings therefore clarified the secretion mechanism of exMPs and provide a novel strategy for further enhancement of exMP production in submerged fermentation.</description><subject>Biosynthetic Pathways</subject><subject>Cell Membrane - genetics</subject><subject>Cell Membrane - metabolism</subject><subject>Cell Membrane Permeability</subject><subject>Ergosterol - biosynthesis</subject><subject>Fermentation</subject><subject>Fungal Proteins - genetics</subject><subject>Fungal Proteins - metabolism</subject><subject>Monascus - genetics</subject><subject>Monascus - metabolism</subject><subject>Pigments, Biological - biosynthesis</subject><issn>0021-8561</issn><issn>1520-5118</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kUtvEzEUhS0EoqGwZ4W8ZNEJfmTszBLS9CG1akRhPbI9d1JXM3bwA8iv46_haVJ2rCxZ3znnHh2E3lMyp4TRT8rE-aPqzbzRpF5K9gLNaM1IVVO6fIlmpDDVshb0BL2J8ZEQsqwleY1OOBVUSipn6M-5jSHvkvUO-x6nB8DrsPUxQfAD_mJ93LvymazBG5Uefqk9_goxDyli6_C1MwFUhA7fwqiDcoA3EEZQ2g427c_wSuVo3Rbf_YSwC77L5ilJuQ7fQ9E-565_p6AMDEMeVMC33qlocsQbux3BHbLusx4hbEvWxRThkprEb9GrXg0R3h3fU_T9Yv1tdVXd3F1erz7fVIpzkaoF5apb1LJvFlwDY8xIU7PecNYooqnQ0GjeaSa4kIwvO6GZXOhykebMNELyU_Tx4Fta_MgQUzvaOB1cOvscW8aJYFRI2hSUHFATfIwB-nYX7KjCvqWknWZry2ztNFt7nK1IPhzdp5LdP8HzTgU4OwBPUp-DK2X_7_cXuUypNA</recordid><startdate>20191211</startdate><enddate>20191211</enddate><creator>Liu, Jun</creator><creator>Chai, Xueying</creator><creator>Guo, Ting</creator><creator>Wu, Jingyan</creator><creator>Yang, Pengpeng</creator><creator>Luo, Yunchuan</creator><creator>Zhao, Hui</creator><creator>Zhao, Wen</creator><creator>Nkechi, Omeoga</creator><creator>Dong, Jie</creator><creator>Bai, Jie</creator><creator>Lin, Qinlu</creator><general>American Chemical Society</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-5322-3916</orcidid></search><sort><creationdate>20191211</creationdate><title>Disruption of the Ergosterol Biosynthetic Pathway Results in Increased Membrane Permeability, Causing Overproduction and Secretion of Extracellular Monascus Pigments in Submerged Fermentation</title><author>Liu, Jun ; Chai, Xueying ; Guo, Ting ; Wu, Jingyan ; Yang, Pengpeng ; Luo, Yunchuan ; Zhao, Hui ; Zhao, Wen ; Nkechi, Omeoga ; Dong, Jie ; Bai, Jie ; Lin, Qinlu</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a336t-413ad457f943be222c7c52fc329a0b16be9b3db26367238d6b274baceb32c9673</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Biosynthetic Pathways</topic><topic>Cell Membrane - genetics</topic><topic>Cell Membrane - metabolism</topic><topic>Cell Membrane Permeability</topic><topic>Ergosterol - biosynthesis</topic><topic>Fermentation</topic><topic>Fungal Proteins - genetics</topic><topic>Fungal Proteins - metabolism</topic><topic>Monascus - genetics</topic><topic>Monascus - metabolism</topic><topic>Pigments, Biological - biosynthesis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Liu, Jun</creatorcontrib><creatorcontrib>Chai, Xueying</creatorcontrib><creatorcontrib>Guo, Ting</creatorcontrib><creatorcontrib>Wu, Jingyan</creatorcontrib><creatorcontrib>Yang, Pengpeng</creatorcontrib><creatorcontrib>Luo, Yunchuan</creatorcontrib><creatorcontrib>Zhao, Hui</creatorcontrib><creatorcontrib>Zhao, Wen</creatorcontrib><creatorcontrib>Nkechi, Omeoga</creatorcontrib><creatorcontrib>Dong, Jie</creatorcontrib><creatorcontrib>Bai, Jie</creatorcontrib><creatorcontrib>Lin, Qinlu</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of agricultural and food chemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Liu, Jun</au><au>Chai, Xueying</au><au>Guo, Ting</au><au>Wu, Jingyan</au><au>Yang, Pengpeng</au><au>Luo, Yunchuan</au><au>Zhao, Hui</au><au>Zhao, Wen</au><au>Nkechi, Omeoga</au><au>Dong, Jie</au><au>Bai, Jie</au><au>Lin, Qinlu</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Disruption of the Ergosterol Biosynthetic Pathway Results in Increased Membrane Permeability, Causing Overproduction and Secretion of Extracellular Monascus Pigments in Submerged Fermentation</atitle><jtitle>Journal of agricultural and food chemistry</jtitle><addtitle>J. Agric. Food Chem</addtitle><date>2019-12-11</date><risdate>2019</risdate><volume>67</volume><issue>49</issue><spage>13673</spage><epage>13683</epage><pages>13673-13683</pages><issn>0021-8561</issn><eissn>1520-5118</eissn><abstract>Because Monascus pigments (MPs) predominantly accumulate in the cytoplasm during submerged fermentation, many biotechnologies are applied to enhance the production of extracellular MPs (exMPs) to reduce the downstream processing costs. In this study, the genes monascus_7017 and monascus_8018, identified as ERG4 genes, were knocked out to disrupt the ergosterol biosynthetic pathway and enhance the production of exMPs in Monascus purpureus LQ-6. Double-deletion of EGR4 in M. purpureus LQ-6 reduced ergosterol concentration by 57.14% and enhanced exMP production 2.06-fold. 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| subjects | Biosynthetic Pathways Cell Membrane - genetics Cell Membrane - metabolism Cell Membrane Permeability Ergosterol - biosynthesis Fermentation Fungal Proteins - genetics Fungal Proteins - metabolism Monascus - genetics Monascus - metabolism Pigments, Biological - biosynthesis |
| title | Disruption of the Ergosterol Biosynthetic Pathway Results in Increased Membrane Permeability, Causing Overproduction and Secretion of Extracellular Monascus Pigments in Submerged Fermentation |
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