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Title: Light regulation of light-harvesting antenna size substantially enhances photosynthetic efficiency and biomass yield in green algae

Abstract

One of the major factors limiting biomass productivity in algae is the low thermodynamic efficiency of photosynthesis. The greatest thermodynamic inefficiencies in photosynthesis occur during the conversion of light into chemical energy. At full sunlight the light-harvesting antenna captures photons at a rate nearly 10 times faster than the rate-limiting step in photosynthetic electron transport. Excess captured energy is dissipated by non-productive pathways including the production of reactive oxygen species. Substantial improvements in photosynthetic efficiency have been achieved by reducing the optical cross-section of the light-harvesting antenna by selectively reducing chlorophyll b levels and peripheral light-harvesting complex subunits. Smaller light-harvesting antenna, however, may not exhibit optimal photosynthetic performance in low or fluctuating light environments. Additionally, we describe a translational control system to dynamically adjust light-harvesting antenna sizes for enhanced photosynthetic performance. Furthermore, by expressing a chlorophyllide a oxygenase (CAO) gene having a 5' mRNA extension encoding a Nab1 translational repressor binding site in a CAO knockout line it was possible to continuously alter chlorophyll b levels and correspondingly light-harvesting antenna sizes by light-activated Nab1 repression of CAO expression as a function of growth light intensity. Significantly, algae having light-regulated antenna sizes had substantially higher photosynthetic rates and two-fold greater biomassmore » productivity than the parental wild-type strains as well as near wild-type ability to carry out state transitions and non-photochemical quenching. These results have broad implications for enhanced algae and plant biomass productivity.« less

Authors:
ORCiD logo [1];  [2];  [3];  [2];  [4];  [4];  [2]; ORCiD logo [5];  [6]; ORCiD logo [7]
  1. Los Alamos National Lab. (LANL), Los Alamos, NM (United States). New Mexico Consortium
  2. Donald Danforth Plant Science Center, St. Louis, MO (United States)
  3. Stanford University Palo Alto CA USA
  4. National Inst. for Basic Biology, Okazaki (Japan); Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency (JST), Okazaki (Japan); Graduate Univ. for Advanced Studies (SOKENDAI), Okazaki (Japan)
  5. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
  6. Univ. of Illinois at Urbana-Champaign, IL (United States)
  7. New Mexico Consortium, Los Alamos, NM (United States)
Publication Date:
Research Org.:
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); U.S. Air Force Office of Scientific Research; Japan Society for the Promotion of Science (JSPS); USDOE Laboratory Directed Research and Development (LDRD) Program
OSTI Identifier:
1645093
Alternate Identifier(s):
OSTI ID: 1615447
Report Number(s):
LA-UR-20-23241
Journal ID: ISSN 0960-7412
Grant/Contract Number:  
89233218CNA000001; SC0001035; 20120535ER; EE0006316; EE0007089; FA9550‐08‐1‐0451; 16H06553; EE00030406; DE‐SC0001035
Resource Type:
Accepted Manuscript
Journal Name:
The Plant Journal
Additional Journal Information:
Journal Volume: 103; Journal Issue: 2; Journal ID: ISSN 0960-7412
Publisher:
Society for Experimental Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Chlamydomonas; algae; photosynthesis; light-harvesting antenna; chlorophyll; thylakoid; non-photochemical quenching; biofuels

Citation Formats

Negi, Sangeeta, Perrine, Zoee, Friedland, Natalia, Kumar, Anil, Tokutsu, Ryutaro, Minagawa, Jun, Berg, Howard, Barry, Amanda N., Govindjee, Govindjee, and Sayre, Richard. Light regulation of light-harvesting antenna size substantially enhances photosynthetic efficiency and biomass yield in green algae. United States: N. p., 2020. Web. https://doi.org/10.1111/tpj.14751.
Negi, Sangeeta, Perrine, Zoee, Friedland, Natalia, Kumar, Anil, Tokutsu, Ryutaro, Minagawa, Jun, Berg, Howard, Barry, Amanda N., Govindjee, Govindjee, & Sayre, Richard. Light regulation of light-harvesting antenna size substantially enhances photosynthetic efficiency and biomass yield in green algae. United States. https://doi.org/10.1111/tpj.14751
Negi, Sangeeta, Perrine, Zoee, Friedland, Natalia, Kumar, Anil, Tokutsu, Ryutaro, Minagawa, Jun, Berg, Howard, Barry, Amanda N., Govindjee, Govindjee, and Sayre, Richard. Tue . "Light regulation of light-harvesting antenna size substantially enhances photosynthetic efficiency and biomass yield in green algae". United States. https://doi.org/10.1111/tpj.14751. https://www.osti.gov/servlets/purl/1645093.
@article{osti_1645093,
title = {Light regulation of light-harvesting antenna size substantially enhances photosynthetic efficiency and biomass yield in green algae},
author = {Negi, Sangeeta and Perrine, Zoee and Friedland, Natalia and Kumar, Anil and Tokutsu, Ryutaro and Minagawa, Jun and Berg, Howard and Barry, Amanda N. and Govindjee, Govindjee and Sayre, Richard},
abstractNote = {One of the major factors limiting biomass productivity in algae is the low thermodynamic efficiency of photosynthesis. The greatest thermodynamic inefficiencies in photosynthesis occur during the conversion of light into chemical energy. At full sunlight the light-harvesting antenna captures photons at a rate nearly 10 times faster than the rate-limiting step in photosynthetic electron transport. Excess captured energy is dissipated by non-productive pathways including the production of reactive oxygen species. Substantial improvements in photosynthetic efficiency have been achieved by reducing the optical cross-section of the light-harvesting antenna by selectively reducing chlorophyll b levels and peripheral light-harvesting complex subunits. Smaller light-harvesting antenna, however, may not exhibit optimal photosynthetic performance in low or fluctuating light environments. Additionally, we describe a translational control system to dynamically adjust light-harvesting antenna sizes for enhanced photosynthetic performance. Furthermore, by expressing a chlorophyllide a oxygenase (CAO) gene having a 5' mRNA extension encoding a Nab1 translational repressor binding site in a CAO knockout line it was possible to continuously alter chlorophyll b levels and correspondingly light-harvesting antenna sizes by light-activated Nab1 repression of CAO expression as a function of growth light intensity. Significantly, algae having light-regulated antenna sizes had substantially higher photosynthetic rates and two-fold greater biomass productivity than the parental wild-type strains as well as near wild-type ability to carry out state transitions and non-photochemical quenching. These results have broad implications for enhanced algae and plant biomass productivity.},
doi = {10.1111/tpj.14751},
journal = {The Plant Journal},
number = 2,
volume = 103,
place = {United States},
year = {2020},
month = {3}
}

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