Enhanced limonene production in cyanobacteria reveals photosynthesis limitations
Terpenes are the major secondary metabolites produced by plants, and have diverse industrial applications as pharmaceuticals, fragrance, solvents, and biofuels. Cyanobacteria are equipped with efficient carbon fixation mechanism, and are ideal cell factories to produce various fuel and chemical prod...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2016-12, Vol.113 (50), p.14225-14230 |
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| creator | Wang, Xin Liu, Wei Xin, Changpeng Zheng, Yi Cheng, Yanbing Sun, Su Li, Runze Zhu, Xin-Guang Dai, Susie Y. Rentzepis, Peter M. Yuan, Joshua S. |
| description | Terpenes are the major secondary metabolites produced by plants, and have diverse industrial applications as pharmaceuticals, fragrance, solvents, and biofuels. Cyanobacteria are equipped with efficient carbon fixation mechanism, and are ideal cell factories to produce various fuel and chemical products. Past efforts to produce terpenes in photosynthetic organisms have gained only limited success. Here we engineered the cyanobacterium Synechococcus elongatus PCC 7942 to efficiently produce limonene through modeling guided study. Computational modeling of limonene flux in response to photosynthetic output has revealed the downstream terpene synthase as a key metabolic flux-controlling node in the MEP (2-C-methyl-D-erythritol 4-phosphate) pathway-derived terpene biosynthesis. By enhancing the downstream limonene carbon sink, we achieved over 100-fold increase in limonene productivity, in contrast to the marginal increase achieved through stepwise metabolic engineering. The establishment of a strong limonene flux revealed potential synergy between photosynthate output and terpene biosynthesis, leading to enhanced carbon flux into the MEP pathway. Moreover, we show that enhanced limonene flux would lead to NADPH accumulation, and slow down photosynthesis electron flow. Fine-tuning ATP/NADPH toward terpene biosynthesis could be a key parameter to adapt photosynthesis to support biofuel/bioproduct production in cyanobacteria. |
| doi_str_mv | 10.1073/pnas.1613340113 |
| format | Article |
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Cyanobacteria are equipped with efficient carbon fixation mechanism, and are ideal cell factories to produce various fuel and chemical products. Past efforts to produce terpenes in photosynthetic organisms have gained only limited success. Here we engineered the cyanobacterium Synechococcus elongatus PCC 7942 to efficiently produce limonene through modeling guided study. Computational modeling of limonene flux in response to photosynthetic output has revealed the downstream terpene synthase as a key metabolic flux-controlling node in the MEP (2-C-methyl-D-erythritol 4-phosphate) pathway-derived terpene biosynthesis. By enhancing the downstream limonene carbon sink, we achieved over 100-fold increase in limonene productivity, in contrast to the marginal increase achieved through stepwise metabolic engineering. The establishment of a strong limonene flux revealed potential synergy between photosynthate output and terpene biosynthesis, leading to enhanced carbon flux into the MEP pathway. Moreover, we show that enhanced limonene flux would lead to NADPH accumulation, and slow down photosynthesis electron flow. Fine-tuning ATP/NADPH toward terpene biosynthesis could be a key parameter to adapt photosynthesis to support biofuel/bioproduct production in cyanobacteria.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1613340113</identifier><identifier>PMID: 27911807</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Adenosine Triphosphate - metabolism ; advanced biofuel ; BASIC BIOLOGICAL SCIENCES ; Biofuels ; Biosynthesis ; Cyanobacteria ; Cyclohexenes - metabolism ; Erythritol - analogs & derivatives ; Erythritol - metabolism ; Hydrocarbons ; Industrial Microbiology ; Kinetics ; limonene ; MEP ; Metabolic Engineering ; Metabolic Networks and Pathways ; Metabolites ; Models, Biological ; NADP - metabolism ; Photosynthesis ; Physical Sciences ; Proteomics ; Sugar Phosphates - metabolism ; Synechococcus - metabolism ; Synechococcus elongatus ; terpene ; Terpenes - metabolism</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2016-12, Vol.113 (50), p.14225-14230</ispartof><rights>Volumes 1–89 and 106–113, copyright as a collective work only; author(s) retains copyright to individual articles</rights><rights>Copyright National Academy of Sciences Dec 13, 2016</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c569t-7119b6e78d8b5202e850d77fc18b33b355cc04924b138ae1be059842e1e4ff8c3</citedby><cites>FETCH-LOGICAL-c569t-7119b6e78d8b5202e850d77fc18b33b355cc04924b138ae1be059842e1e4ff8c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26472820$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26472820$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27901,27902,53766,53768,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27911807$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/servlets/purl/1465396$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Xin</creatorcontrib><creatorcontrib>Liu, Wei</creatorcontrib><creatorcontrib>Xin, Changpeng</creatorcontrib><creatorcontrib>Zheng, Yi</creatorcontrib><creatorcontrib>Cheng, Yanbing</creatorcontrib><creatorcontrib>Sun, Su</creatorcontrib><creatorcontrib>Li, Runze</creatorcontrib><creatorcontrib>Zhu, Xin-Guang</creatorcontrib><creatorcontrib>Dai, Susie Y.</creatorcontrib><creatorcontrib>Rentzepis, Peter M.</creatorcontrib><creatorcontrib>Yuan, Joshua S.</creatorcontrib><creatorcontrib>Texas Agrilife Research, College Station, TX (United States)</creatorcontrib><title>Enhanced limonene production in cyanobacteria reveals photosynthesis limitations</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Terpenes are the major secondary metabolites produced by plants, and have diverse industrial applications as pharmaceuticals, fragrance, solvents, and biofuels. Cyanobacteria are equipped with efficient carbon fixation mechanism, and are ideal cell factories to produce various fuel and chemical products. Past efforts to produce terpenes in photosynthetic organisms have gained only limited success. Here we engineered the cyanobacterium Synechococcus elongatus PCC 7942 to efficiently produce limonene through modeling guided study. Computational modeling of limonene flux in response to photosynthetic output has revealed the downstream terpene synthase as a key metabolic flux-controlling node in the MEP (2-C-methyl-D-erythritol 4-phosphate) pathway-derived terpene biosynthesis. By enhancing the downstream limonene carbon sink, we achieved over 100-fold increase in limonene productivity, in contrast to the marginal increase achieved through stepwise metabolic engineering. The establishment of a strong limonene flux revealed potential synergy between photosynthate output and terpene biosynthesis, leading to enhanced carbon flux into the MEP pathway. Moreover, we show that enhanced limonene flux would lead to NADPH accumulation, and slow down photosynthesis electron flow. Fine-tuning ATP/NADPH toward terpene biosynthesis could be a key parameter to adapt photosynthesis to support biofuel/bioproduct production in cyanobacteria.</description><subject>Adenosine Triphosphate - metabolism</subject><subject>advanced biofuel</subject><subject>BASIC BIOLOGICAL SCIENCES</subject><subject>Biofuels</subject><subject>Biosynthesis</subject><subject>Cyanobacteria</subject><subject>Cyclohexenes - metabolism</subject><subject>Erythritol - analogs & derivatives</subject><subject>Erythritol - metabolism</subject><subject>Hydrocarbons</subject><subject>Industrial Microbiology</subject><subject>Kinetics</subject><subject>limonene</subject><subject>MEP</subject><subject>Metabolic Engineering</subject><subject>Metabolic Networks and Pathways</subject><subject>Metabolites</subject><subject>Models, Biological</subject><subject>NADP - metabolism</subject><subject>Photosynthesis</subject><subject>Physical Sciences</subject><subject>Proteomics</subject><subject>Sugar Phosphates - metabolism</subject><subject>Synechococcus - metabolism</subject><subject>Synechococcus elongatus</subject><subject>terpene</subject><subject>Terpenes - metabolism</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkc1v1DAQxSMEotvCmRMogguXbWf8kTiXSqhqAakSHOBsOc6EeJW1g-1U2v-eRFta4MRpDvN7bz5eUbxCOEeo-cXkTTrHCjkXgMifFBuEBreVaOBpsQFg9VYJJk6K05R2ANBIBc-LE1Y3iArqTfH12g_GW-rK0e2DJ0_lFEM32-yCL50v7cH40BqbKTpTRrojM6ZyGkIO6eDzQMmlVeuyWSXpRfGsXwh6eV_Piu8319-uPm1vv3z8fPXhdmtl1eRtjdi0FdWqU61kwEhJ6Oq6t6hazlsupbUgGiZa5MoQtgSyWU4hJNH3yvKz4vLoO83tnjpLPkcz6im6vYkHHYzTf3e8G_SPcKclVjUKWAzeHg1Cyk4n6zLZwQbvyWaNopK8qRbo_f2UGH7OlLLeu2RpHI2nMCeNquIMl0XxP1AhFWcMVtd3_6C7MEe_vGuhJILiHFbDiyNlY0gpUv9wHIJe09dr-vox_UXx5s-fPPC_416A10dgl3KIj_1K1Ewx4L8AS7O1TQ</recordid><startdate>20161213</startdate><enddate>20161213</enddate><creator>Wang, Xin</creator><creator>Liu, Wei</creator><creator>Xin, Changpeng</creator><creator>Zheng, Yi</creator><creator>Cheng, Yanbing</creator><creator>Sun, Su</creator><creator>Li, Runze</creator><creator>Zhu, Xin-Guang</creator><creator>Dai, Susie Y.</creator><creator>Rentzepis, Peter M.</creator><creator>Yuan, Joshua S.</creator><general>National Academy of Sciences</general><general>National Academy of Sciences, Washington, DC (United States)</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>OIOZB</scope><scope>OTOTI</scope><scope>5PM</scope></search><sort><creationdate>20161213</creationdate><title>Enhanced limonene production in cyanobacteria reveals photosynthesis limitations</title><author>Wang, Xin ; 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Cyanobacteria are equipped with efficient carbon fixation mechanism, and are ideal cell factories to produce various fuel and chemical products. Past efforts to produce terpenes in photosynthetic organisms have gained only limited success. Here we engineered the cyanobacterium Synechococcus elongatus PCC 7942 to efficiently produce limonene through modeling guided study. Computational modeling of limonene flux in response to photosynthetic output has revealed the downstream terpene synthase as a key metabolic flux-controlling node in the MEP (2-C-methyl-D-erythritol 4-phosphate) pathway-derived terpene biosynthesis. By enhancing the downstream limonene carbon sink, we achieved over 100-fold increase in limonene productivity, in contrast to the marginal increase achieved through stepwise metabolic engineering. The establishment of a strong limonene flux revealed potential synergy between photosynthate output and terpene biosynthesis, leading to enhanced carbon flux into the MEP pathway. Moreover, we show that enhanced limonene flux would lead to NADPH accumulation, and slow down photosynthesis electron flow. Fine-tuning ATP/NADPH toward terpene biosynthesis could be a key parameter to adapt photosynthesis to support biofuel/bioproduct production in cyanobacteria.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>27911807</pmid><doi>10.1073/pnas.1613340113</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Adenosine Triphosphate - metabolism advanced biofuel BASIC BIOLOGICAL SCIENCES Biofuels Biosynthesis Cyanobacteria Cyclohexenes - metabolism Erythritol - analogs & derivatives Erythritol - metabolism Hydrocarbons Industrial Microbiology Kinetics limonene MEP Metabolic Engineering Metabolic Networks and Pathways Metabolites Models, Biological NADP - metabolism Photosynthesis Physical Sciences Proteomics Sugar Phosphates - metabolism Synechococcus - metabolism Synechococcus elongatus terpene Terpenes - metabolism |
| title | Enhanced limonene production in cyanobacteria reveals photosynthesis limitations |
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