Analysis and modification of central carbon metabolism in Hypsizygus marmoreus for improving mycelial growth performance and fruiting body yield
Hypsizygus marmoreus is one of the main industrially cultivated varieties of edible fungi, with a delicious taste and high nutritional value. However, the long harvest period of 130–150 days greatly limits its large-scale expansion. This study aimed to investigate the effects of central carbon metab...
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Frontiers Media S.A.
2023-07-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1233512/full |
| _version_ | 1797772920102060032 |
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| author | Hui Lin Hui Lin Pengfei Li Lu Ma Shufang Lai Shujing Sun Kaihui Hu Liaoyuan Zhang |
| author_facet | Hui Lin Hui Lin Pengfei Li Lu Ma Shufang Lai Shujing Sun Kaihui Hu Liaoyuan Zhang |
| author_sort | Hui Lin |
| collection | DOAJ |
| description | Hypsizygus marmoreus is one of the main industrially cultivated varieties of edible fungi, with a delicious taste and high nutritional value. However, the long harvest period of 130–150 days greatly limits its large-scale expansion. This study aimed to investigate the effects of central carbon metabolism (CCM) on the mycelial growth performance and fruiting body formation of H. marmoreus. Nine edible fungi with different harvest periods were collected and used to evaluate their intracellular carbon metabolic differences in the CCM, which revealed that the imbalanced distribution of intracellular carbon metabolic levels in the CCM of H. marmoreus might be one of the key factors resulting in a slow mycelial growth rate and a long harvest period. Further analysis by three strategies, including metabolomics, adaptation of different carbon sources, and chemical interference, confirmed that low carbon flux into the pentose phosphate pathway (PPP) limited the supply of raw materials, reduced power, and thus influenced the mycelial growth of H. marmoreus. Furthermore, four transformants with increased expression levels of glucose-6-phosphate dehydrogenase (G6PDH), a key rate-limiting enzyme in the PPP of H. marmoreus, were developed and showed more extracellular soluble protein secretion and higher sugar assimilation rates, as well as improved mycelial growth rates in bottle substrate mixtures. Finally, cultivation experiments indicated that the maturation periods of the fruiting body with ~4–5 days in advance and the maximum fruiting body yield of 574.8 g per bag with an increase of 7.4% were achieved by improving the G6PDH expression level of the PPP in H. marmoreus. This study showed that CCM played an important role in the mycelial growth and development of H. marmoreus, which provided new insights for future advancements in cultivating and breeding edible fungi. |
| first_indexed | 2024-03-12T21:58:47Z |
| format | Article |
| id | doaj.art-2ec97c21d8a84873acd96711e6e26aa5 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-03-12T21:58:47Z |
| publishDate | 2023-07-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-2ec97c21d8a84873acd96711e6e26aa52023-07-25T11:00:47ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-07-011410.3389/fmicb.2023.12335121233512Analysis and modification of central carbon metabolism in Hypsizygus marmoreus for improving mycelial growth performance and fruiting body yieldHui Lin0Hui Lin1Pengfei Li2Lu Ma3Shufang Lai4Shujing Sun5Kaihui Hu6Liaoyuan Zhang7Department of Bioengineering, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, Fujian, ChinaInstitute of Edible Fungi, Fujian Academy of Agricultural Sciences, Fuzhou, Fujian, ChinaDepartment of Bioengineering, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, Fujian, ChinaInstitute of Edible Fungi, Fujian Academy of Agricultural Sciences, Fuzhou, Fujian, ChinaFujian Edible Fungus Technology Promotion General Station, Fuzhou, Fujian, ChinaDepartment of Bioengineering, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, Fujian, ChinaDepartment of Bioengineering, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, Fujian, ChinaDepartment of Bioengineering, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, Fujian, ChinaHypsizygus marmoreus is one of the main industrially cultivated varieties of edible fungi, with a delicious taste and high nutritional value. However, the long harvest period of 130–150 days greatly limits its large-scale expansion. This study aimed to investigate the effects of central carbon metabolism (CCM) on the mycelial growth performance and fruiting body formation of H. marmoreus. Nine edible fungi with different harvest periods were collected and used to evaluate their intracellular carbon metabolic differences in the CCM, which revealed that the imbalanced distribution of intracellular carbon metabolic levels in the CCM of H. marmoreus might be one of the key factors resulting in a slow mycelial growth rate and a long harvest period. Further analysis by three strategies, including metabolomics, adaptation of different carbon sources, and chemical interference, confirmed that low carbon flux into the pentose phosphate pathway (PPP) limited the supply of raw materials, reduced power, and thus influenced the mycelial growth of H. marmoreus. Furthermore, four transformants with increased expression levels of glucose-6-phosphate dehydrogenase (G6PDH), a key rate-limiting enzyme in the PPP of H. marmoreus, were developed and showed more extracellular soluble protein secretion and higher sugar assimilation rates, as well as improved mycelial growth rates in bottle substrate mixtures. Finally, cultivation experiments indicated that the maturation periods of the fruiting body with ~4–5 days in advance and the maximum fruiting body yield of 574.8 g per bag with an increase of 7.4% were achieved by improving the G6PDH expression level of the PPP in H. marmoreus. This study showed that CCM played an important role in the mycelial growth and development of H. marmoreus, which provided new insights for future advancements in cultivating and breeding edible fungi.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1233512/fullHypsizygus marmoreusharvest periodcentral carbon metabolism (CCM)pentose phosphate pathway (PPP)glucose-6-phosphate dehydrogenase (G6PDH) |
| spellingShingle | Hui Lin Hui Lin Pengfei Li Lu Ma Shufang Lai Shujing Sun Kaihui Hu Liaoyuan Zhang Analysis and modification of central carbon metabolism in Hypsizygus marmoreus for improving mycelial growth performance and fruiting body yield Frontiers in Microbiology Hypsizygus marmoreus harvest period central carbon metabolism (CCM) pentose phosphate pathway (PPP) glucose-6-phosphate dehydrogenase (G6PDH) |
| title | Analysis and modification of central carbon metabolism in Hypsizygus marmoreus for improving mycelial growth performance and fruiting body yield |
| title_full | Analysis and modification of central carbon metabolism in Hypsizygus marmoreus for improving mycelial growth performance and fruiting body yield |
| title_fullStr | Analysis and modification of central carbon metabolism in Hypsizygus marmoreus for improving mycelial growth performance and fruiting body yield |
| title_full_unstemmed | Analysis and modification of central carbon metabolism in Hypsizygus marmoreus for improving mycelial growth performance and fruiting body yield |
| title_short | Analysis and modification of central carbon metabolism in Hypsizygus marmoreus for improving mycelial growth performance and fruiting body yield |
| title_sort | analysis and modification of central carbon metabolism in hypsizygus marmoreus for improving mycelial growth performance and fruiting body yield |
| topic | Hypsizygus marmoreus harvest period central carbon metabolism (CCM) pentose phosphate pathway (PPP) glucose-6-phosphate dehydrogenase (G6PDH) |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1233512/full |
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