Nannochloropsis, a rich source of diacylglycerol acyltransferases for engineering of triacylglycerol content in different hosts

Zienkiewicz, Krzysztof; Zienkiewicz, Agnieszka; Poliner, Eric; Du, Zhi-Yan; Vollheyde, Katharina; Herrfurth, Cornelia; Marmon, Sofia; Farré, Eva M.; Feussner, Ivo; Benning, Christoph

doi:10.1186/s13068-016-0686-8

Title: Nannochloropsis, a rich source of diacylglycerol acyltransferases for engineering of triacylglycerol content in different hosts

Abstract

Photosynthetic microalgae are considered a viable and sustainable resource for biofuel feedstocks, because they can produce higher biomass per land area than plants and can be grown on non-arable land. Among many microalgae considered for biofuel production, Nannochloropsis oceanica (CCMP1779) is particularly promising, because following nutrient deprivation it produces very high amounts of triacylglycerols (TAG). The committed step in TAG synthesis is catalyzed by acyl-CoA:diacylglycerol acyltransferase (DGAT). Remarkably, a total of 13 putative DGAT-encoding genes have been previously identified in CCMP1779 but most have not yet been studied in detail. We chose six out of 12 type-2 DGAT-encoding genes (NoDGTT1-NoDGTT6), based on their expression profile, for their possible role in TAG biosynthesis and the respective cDNAs were expressed in a TAG synthesis-deficient mutant of yeast. Yeast expressing NoDGTT5 accumulated TAG to the highest level. Over-expression of NoDGTT5 in CCMP1779 grown in N-replete medium resulted in levels of TAG normally observed only after N deprivation. Reduced growth rates accompanied NoDGTT5 over-expression in CCMP1779. Constitutive expression of NoDGTT5 in Arabidopsis thaliana was accompanied by increased TAG content in seeds and leaves. A broad substrate specificity for NoDGTT5 was revealed, with preference for unsaturated acyl groups. Furthermore, NoDGTT5 was able to successfully rescuemore »« less

Authors:

; Zienkiewicz, Agnieszka; Poliner, Eric; Du, Zhi-Yan; Vollheyde, Katharina; Herrfurth, Cornelia; Marmon, Sofia; Farré, Eva M.; Feussner, Ivo; Benning, Christoph

Publication Date:: Tue Jan 03 00:00:00 EST 2017

Research Org.:: Michigan State Univ., East Lansing, MI (United States); Univ. of Wisconsin, Madison, WI (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

OSTI Identifier:: 1618806

Alternate Identifier(s):: OSTI ID: 1366477

Grant/Contract Number:: DE–FG02–91ER20021; FC02-07ER64494; FG02-91ER20021

Resource Type:: Published Article

Journal Name:: Biotechnology for Biofuels

Additional Journal Information:: Journal Name: Biotechnology for Biofuels Journal Volume: 10 Journal Issue: 1; Journal ID: ISSN 1754-6834

Publisher:: Springer Science + Business Media

Country of Publication:: Netherlands

Language:: English

Subject:: 60 APPLIED LIFE SCIENCES; 09 BIOMASS FUELS; Nannochloropsis oceanica; Microalgae; DGAT; Triacylglycerol; Lipid storage; Lipid droplets

Citation Formats


                    Zienkiewicz, Krzysztof, Zienkiewicz, Agnieszka, Poliner, Eric, Du, Zhi-Yan, Vollheyde, Katharina, Herrfurth, Cornelia, Marmon, Sofia, Farré, Eva M., Feussner, Ivo, and Benning, Christoph. Nannochloropsis, a rich source of diacylglycerol acyltransferases for engineering of triacylglycerol content in different hosts.  Netherlands: N. p., 2017. 
Web.  doi:10.1186/s13068-016-0686-8.

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                    Zienkiewicz, Krzysztof, Zienkiewicz, Agnieszka, Poliner, Eric, Du, Zhi-Yan, Vollheyde, Katharina, Herrfurth, Cornelia, Marmon, Sofia, Farré, Eva M., Feussner, Ivo, & Benning, Christoph. Nannochloropsis, a rich source of diacylglycerol acyltransferases for engineering of triacylglycerol content in different hosts.  Netherlands.  https://doi.org/10.1186/s13068-016-0686-8

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                    Zienkiewicz, Krzysztof, Zienkiewicz, Agnieszka, Poliner, Eric, Du, Zhi-Yan, Vollheyde, Katharina, Herrfurth, Cornelia, Marmon, Sofia, Farré, Eva M., Feussner, Ivo, and Benning, Christoph. Tue .  
"Nannochloropsis, a rich source of diacylglycerol acyltransferases for engineering of triacylglycerol content in different hosts".  Netherlands.  https://doi.org/10.1186/s13068-016-0686-8.

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@article{osti_1618806,

  title        = {Nannochloropsis, a rich source of diacylglycerol acyltransferases for engineering of triacylglycerol content in different hosts},

  author       = {Zienkiewicz, Krzysztof and Zienkiewicz, Agnieszka and Poliner, Eric and Du, Zhi-Yan and Vollheyde, Katharina and Herrfurth, Cornelia and Marmon, Sofia and Farré, Eva M. and Feussner, Ivo and Benning, Christoph},

  abstractNote = {Photosynthetic microalgae are considered a viable and sustainable resource for biofuel feedstocks, because they can produce higher biomass per land area than plants and can be grown on non-arable land. Among many microalgae considered for biofuel production, Nannochloropsis oceanica (CCMP1779) is particularly promising, because following nutrient deprivation it produces very high amounts of triacylglycerols (TAG). The committed step in TAG synthesis is catalyzed by acyl-CoA:diacylglycerol acyltransferase (DGAT). Remarkably, a total of 13 putative DGAT-encoding genes have been previously identified in CCMP1779 but most have not yet been studied in detail. We chose six out of 12 type-2 DGAT-encoding genes (NoDGTT1-NoDGTT6), based on their expression profile, for their possible role in TAG biosynthesis and the respective cDNAs were expressed in a TAG synthesis-deficient mutant of yeast. Yeast expressing NoDGTT5 accumulated TAG to the highest level. Over-expression of NoDGTT5 in CCMP1779 grown in N-replete medium resulted in levels of TAG normally observed only after N deprivation. Reduced growth rates accompanied NoDGTT5 over-expression in CCMP1779. Constitutive expression of NoDGTT5 in Arabidopsis thaliana was accompanied by increased TAG content in seeds and leaves. A broad substrate specificity for NoDGTT5 was revealed, with preference for unsaturated acyl groups. Furthermore, NoDGTT5 was able to successfully rescue the Arabidopsis tag1-1 mutant by restoring the TAG content in seeds. Taken together, these results identified NoDGTT5 as the most promising gene for the engineering of TAG synthesis in multiple hosts among the 13 DGAT-encoding genes of N. oceanica CCMP1779. Consequently, this study demonstrates the potential of NoDGTT5 as a tool for enhancing the energy density in biomass by increasing TAG content in transgenic crops used for biofuel production.},

  doi          = {10.1186/s13068-016-0686-8},

  journal      = {Biotechnology for Biofuels},

  number       = 1,

  volume       = 10,

  place        = {Netherlands},

  year         = {Tue Jan 03 00:00:00 EST 2017},

  month        = {Tue Jan 03 00:00:00 EST 2017}

}

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A toolkit for Nannochloropsis oceanica CCMP1779 enables gene stacking and genetic engineering of the eicosapentaenoic acid pathway for enhanced long-chain polyunsaturated fatty acid production

Journal Article Poliner, Eric ; Pulman, Jane A. ; Zienkiewicz, Krzysztof ; ... - Plant Biotechnology Journal

Nannochloropsis oceanica is an oleaginous microalga rich in ω3 long-chain polyunsaturated fatty acids (LC-PUFAs) content, in the form of eicosapentaenoic acid (EPA). We identified the enzymes involved in LC-PUFA biosynthesis in N. oceanica CCMP1779 and generated multigene expression vectors aiming at increasing LC-PUFA content in vivo. We isolated the cDNAs encoding four fatty acid desaturases (FAD) and determined their function by heterologous expression in S. cerevisiae. To increase the expression of multiple fatty acid desaturases in N. oceanica CCMP1779, we developed a genetic engineering toolkit that includes an endogenous bidirectional promoter and optimized peptide bond skipping 2A peptides. The toolkitmore »« less
Cited by 81
https://doi.org/10.1111/pbi.12772
Generation of camelina mid-oleic acid seed oil by identification and stacking of fatty acid biosynthetic mutants

Journal Article Neumann, Nicholas G. ; Nazarenus, Tara J. ; Aznar-Moreno, Jose A. ; ... - Industrial Crops and Products

Modifying oilseeds to obtain a desired fatty acid composition is often necessary to enable use as feedstocks for specific applications such as food processing, biofuels, or biolubricants. A mutant population of camelina (Camelina sativa), an emerging specialty oilseed crop, was screened by high-throughput gas chromatography for lines with altered seed oil fatty acid composition. By leveraging knowledge of fatty acid synthesis in Arabidopsis thaliana, mutations in orthologs of FATTY ACID ELONGASE1 (FAE1), FATTY ACID DESATURASE2 (FAD2), FATTY ACID DESATURASE3 (FAD3), and β-KETO-ACYL-ACP SYNTHASE II (KASII; FAB1) were identified. The mutations altered conserved amino acid residues in the encoded proteins. Themore »« less
https://doi.org/10.1016/j.indcrop.2020.113074

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Engineering the production of conjugated fatty acids in Arabidopsis thaliana leaves

Journal Article Yurchenko, Olga ; Shockey, Jay M. ; Gidda, Satinder K. ; ... - Plant Biotechnology Journal

Summary The seeds of many nondomesticated plant species synthesize oils containing high amounts of a single unusual fatty acid, many of which have potential usage in industry. Despite the identification of enzymes for unusual oxidized fatty acid synthesis, the production of these fatty acids in engineered seeds remains low and is often hampered by their inefficient exclusion from phospholipids. Recent studies have established the feasibility of increasing triacylglycerol content in plant leaves, which provides a novel approach for increasing energy density of biomass crops. Here, we determined whether the fatty acid composition of leaf oil could be engineered to accumulatemore »« less
Cited by 25
https://doi.org/10.1111/pbi.12695
The Microalga Nannochloropsis during Transition from Quiescence to Autotrophy in Response to Nitrogen Availability

Journal Article Zienkiewicz, Agnieszka ; Zienkiewicz, Krzysztof ; Poliner, Eric ; ... - Plant Physiology (Bethesda)

The marine microalgae Nannochloropsis oceanica (CCMP1779) is a prolific producer of oil and is considered a viable and sustainable resource for biofuel feedstocks. Nitrogen (N) availability has a strong impact on the physiological status and metabolism of microalgal cells, but the exact nature of this response is poorly understood. To fill this gap we performed transcriptomic profiling combined with cellular and molecular analyses of N. oceanica CCMP1779 during the transition from quiescence to autotrophy. N deprivation-induced quiescence was accompanied by a strong reorganization of the photosynthetic apparatus and changes in the lipid homeostasis, leading to accumulation of triacylglycerol. Cell cyclemore »« less
Cited by 40
https://doi.org/10.1104/pp.19.00854

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