The Microalga Nannochloropsis during Transition from Quiescence to Autotrophy in Response to Nitrogen Availability

Zienkiewicz, Agnieszka; Zienkiewicz, Krzysztof; Poliner, Eric; Pulman, Jane A.; Du, Zhi-Yan; Stefano, Giovanni; Tsai, Chia-Hong; Horn, Patrick; Feussner, Ivo; Farre, Eva M.; Childs, Kevin L.; Brandizzi, Federica; Benning, Christoph

doi:10.1104/pp.19.00854

Title: The Microalga Nannochloropsis during Transition from Quiescence to Autotrophy in Response to Nitrogen Availability

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Abstract

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 cycle activation and reestablishment of photosynthetic activity observed in response to resupply of the growth medium with N were accompanied by a rapid degradation of triacylglycerol stored in lipid droplets (LDs). Besides observing LD translocation into vacuoles, we also provide evidence for direct interaction between the LD surface protein (NoLDSP) and AUTOPHAGY-RELATED8 (NoATG8) protein and show a role of microlipophagy in LD turnover in N. oceanica CCMP1779. This knowledge is crucial not only for understanding the fundamental mechanisms controlling the cellular energy homeostasis in microalgal cells but also for development of efficient strategies to achieve higher algal biomass and better microalgalmore » lipid productivity.« less

Authors:

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^[2]; Poliner, Eric ^[3]; Pulman, Jane A. ^[4];

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^[5]; Tsai, Chia-Hong ^[6];

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Michigan State University-United States Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, Michigan 48824, Great Lakes Bioenergy Center, Michigan State University, East Lansing, Michigan 48824, Centre for Modern Interdisciplinary Technologies, Nicolaus Copernicus University, 87-100 Toruń, Poland
Michigan State University-United States Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, Michigan 48824, Centre for Modern Interdisciplinary Technologies, Nicolaus Copernicus University, 87-100 Toruń, Poland, Department of Plant Biochemistry, Albrecht-von-Haller-Institute for Plant Sciences, University of Goettingen, 37073 Goettingen, Germany
Michigan State University-United States Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, Michigan 48824, Cell and Molecular Biology Program, Michigan State University, East Lansing, Michigan 48824, Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824
Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824, Center for Genomics-Enabled Plant Science, Michigan State University, East Lansing, Michigan 48824
Michigan State University-United States Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, Michigan 48824
Michigan State University-United States Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, Michigan 48824, Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824
Department of Plant Biochemistry, Albrecht-von-Haller-Institute for Plant Sciences, University of Goettingen, 37073 Goettingen, Germany, Department of Plant Biochemistry, Goettingen Center for Molecular Biosciences (GZMB), University of Goettingen, 37073 Goettingen, Germany, Department of Plant Biochemistry, International Center for Advanced Studies of Energy Conversion (ICASEC), University of Goettingen, 37073 Goettingen, Germany
Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824
Michigan State University-United States Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, Michigan 48824, Great Lakes Bioenergy Center, Michigan State University, East Lansing, Michigan 48824, Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824, Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824

Publication Date:: Mon Nov 18 00:00:00 EST 2019

Research Org.:: Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory

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

OSTI Identifier:: 1574533

Alternate Identifier(s):: OSTI ID: 1735509

Grant/Contract Number:: FC02-07ER64494; FG02-91ER20021; MCB1714561; IOS-1354721

Resource Type:: Published Article

Journal Name:: Plant Physiology (Bethesda)

Additional Journal Information:: Journal Name: Plant Physiology (Bethesda) Journal Volume: 182 Journal Issue: 2; Journal ID: ISSN 0032-0889

Publisher:: American Society of Plant Biologists

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Zienkiewicz, Agnieszka, Zienkiewicz, Krzysztof, Poliner, Eric, Pulman, Jane A., Du, Zhi-Yan, Stefano, Giovanni, Tsai, Chia-Hong, Horn, Patrick, Feussner, Ivo, Farre, Eva M., Childs, Kevin L., Brandizzi, Federica, and Benning, Christoph. The Microalga Nannochloropsis during Transition from Quiescence to Autotrophy in Response to Nitrogen Availability.  United States: N. p., 2019. 
Web.  doi:10.1104/pp.19.00854.

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                    Zienkiewicz, Agnieszka, Zienkiewicz, Krzysztof, Poliner, Eric, Pulman, Jane A., Du, Zhi-Yan, Stefano, Giovanni, Tsai, Chia-Hong, Horn, Patrick, Feussner, Ivo, Farre, Eva M., Childs, Kevin L., Brandizzi, Federica, & Benning, Christoph. The Microalga Nannochloropsis during Transition from Quiescence to Autotrophy in Response to Nitrogen Availability.  United States.  https://doi.org/10.1104/pp.19.00854

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                    Zienkiewicz, Agnieszka, Zienkiewicz, Krzysztof, Poliner, Eric, Pulman, Jane A., Du, Zhi-Yan, Stefano, Giovanni, Tsai, Chia-Hong, Horn, Patrick, Feussner, Ivo, Farre, Eva M., Childs, Kevin L., Brandizzi, Federica, and Benning, Christoph. Mon .  
"The Microalga Nannochloropsis during Transition from Quiescence to Autotrophy in Response to Nitrogen Availability".  United States.  https://doi.org/10.1104/pp.19.00854.

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@article{osti_1574533,

  title        = {The Microalga Nannochloropsis during Transition from Quiescence to Autotrophy in Response to Nitrogen Availability},

  author       = {Zienkiewicz, Agnieszka and Zienkiewicz, Krzysztof and Poliner, Eric and Pulman, Jane A. and Du, Zhi-Yan and Stefano, Giovanni and Tsai, Chia-Hong and Horn, Patrick and Feussner, Ivo and Farre, Eva M. and Childs, Kevin L. and Brandizzi, Federica and Benning, Christoph},

  abstractNote = {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 cycle activation and reestablishment of photosynthetic activity observed in response to resupply of the growth medium with N were accompanied by a rapid degradation of triacylglycerol stored in lipid droplets (LDs). Besides observing LD translocation into vacuoles, we also provide evidence for direct interaction between the LD surface protein (NoLDSP) and AUTOPHAGY-RELATED8 (NoATG8) protein and show a role of microlipophagy in LD turnover in N. oceanica CCMP1779. This knowledge is crucial not only for understanding the fundamental mechanisms controlling the cellular energy homeostasis in microalgal cells but also for development of efficient strategies to achieve higher algal biomass and better microalgal lipid productivity.},

  doi          = {10.1104/pp.19.00854},

  journal      = {Plant Physiology (Bethesda)},

  number       = 2,

  volume       = 182,

  place        = {United States},

  year         = {Mon Nov 18 00:00:00 EST 2019},

  month        = {Mon Nov 18 00:00:00 EST 2019}

}

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