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Title: Cyanobacterial Alkanes Modulate Photosynthetic Cyclic Electron Flow to Assist Growth under Cold Stress

Abstract

All cyanobacterial membranes contain diesel-range C15-C19 hydrocarbons at concentrations similar to chlorophyll. Recently, two universal but mutually exclusive hydrocarbon production pathways in cyanobacteria were discovered. We engineered a mutant of Synechocystis sp. PCC 6803 that produces no alkanes, which grew poorly at low temperatures. We analyzed this defect by assessing the redox kinetics of PSI. The mutant exhibited enhanced cyclic electron flow (CEF), especially at low temperature. CEF raises the ATP:NADPH ratio from photosynthesis and balances reductant requirements of biosynthesis with maintaining the redox poise of the electron transport chain. We conducted in silico flux balance analysis and showed that growth rate reaches a distinct maximum for an intermediate value of CEF equivalent to recycling 1 electron in 4 from PSI to the plastoquinone pool. Based on this analysis, we conclude that the lack of membrane alkanes causes higher CEF, perhaps for maintenance of redox poise. In turn, increased CEF reduces growth by forcing the cell to use less energy-efficient pathways, lowering the quantum efficiency of photosynthesis. This study highlights the unique and universal role of medium-chain hydrocarbons in cyanobacterial thylakoid membranes: they regulate redox balance and reductant partitioning in these oxygenic photosynthetic cells under stress.

Authors:
 [1];  [2];  [3];  [4]
  1. Washington Univ., St. Louis, MO (United States). Dept. of Energy, Environmental, and Chemical Engineering
  2. Washington Univ., St. Louis, MO (United States). Dept. of Biology; Pennsylvania State Univ., University Park, PA (United States). Dept. of Chemical Engineering
  3. Pennsylvania State Univ., University Park, PA (United States). Dept. of Chemical Engineering
  4. Washington Univ., St. Louis, MO (United States). Dept. of Energy, Environmental, and Chemical Engineering; Washington Univ., St. Louis, MO (United States). Dept. of Biology
Publication Date:
Research Org.:
Washington Univ., St. Louis, MO (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1624800
Grant/Contract Number:  
FG02-00ER41132
Resource Type:
Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 5; Journal Issue: 1; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Science & Technology - Other Topics

Citation Formats

Berla, Bertram M., Saha, Rajib, Maranas, Costas D., and Pakrasi, Himadri B. Cyanobacterial Alkanes Modulate Photosynthetic Cyclic Electron Flow to Assist Growth under Cold Stress. United States: N. p., 2015. Web. doi:10.1038/srep14894.
Berla, Bertram M., Saha, Rajib, Maranas, Costas D., & Pakrasi, Himadri B. Cyanobacterial Alkanes Modulate Photosynthetic Cyclic Electron Flow to Assist Growth under Cold Stress. United States. https://doi.org/10.1038/srep14894
Berla, Bertram M., Saha, Rajib, Maranas, Costas D., and Pakrasi, Himadri B. Tue . "Cyanobacterial Alkanes Modulate Photosynthetic Cyclic Electron Flow to Assist Growth under Cold Stress". United States. https://doi.org/10.1038/srep14894. https://www.osti.gov/servlets/purl/1624800.
@article{osti_1624800,
title = {Cyanobacterial Alkanes Modulate Photosynthetic Cyclic Electron Flow to Assist Growth under Cold Stress},
author = {Berla, Bertram M. and Saha, Rajib and Maranas, Costas D. and Pakrasi, Himadri B.},
abstractNote = {All cyanobacterial membranes contain diesel-range C15-C19 hydrocarbons at concentrations similar to chlorophyll. Recently, two universal but mutually exclusive hydrocarbon production pathways in cyanobacteria were discovered. We engineered a mutant of Synechocystis sp. PCC 6803 that produces no alkanes, which grew poorly at low temperatures. We analyzed this defect by assessing the redox kinetics of PSI. The mutant exhibited enhanced cyclic electron flow (CEF), especially at low temperature. CEF raises the ATP:NADPH ratio from photosynthesis and balances reductant requirements of biosynthesis with maintaining the redox poise of the electron transport chain. We conducted in silico flux balance analysis and showed that growth rate reaches a distinct maximum for an intermediate value of CEF equivalent to recycling 1 electron in 4 from PSI to the plastoquinone pool. Based on this analysis, we conclude that the lack of membrane alkanes causes higher CEF, perhaps for maintenance of redox poise. In turn, increased CEF reduces growth by forcing the cell to use less energy-efficient pathways, lowering the quantum efficiency of photosynthesis. This study highlights the unique and universal role of medium-chain hydrocarbons in cyanobacterial thylakoid membranes: they regulate redox balance and reductant partitioning in these oxygenic photosynthetic cells under stress.},
doi = {10.1038/srep14894},
journal = {Scientific Reports},
number = 1,
volume = 5,
place = {United States},
year = {Tue Oct 13 00:00:00 EDT 2015},
month = {Tue Oct 13 00:00:00 EDT 2015}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Figures / Tables:

Figure 1 Figure 1: Cartoon of cyanobacterial photosynthetic electron transport pathways. In the linear electron transport pathway (dotted magenta line), light is first absorbed by PSII, then excited electrons are transported inside the membrane by PQ to the cyt b6f complex, then through the thylakoid lumen by the PC to PSI. Atmore » PSI, electrons are excited by light a second time and then reduce NADP+. Along the way, protons are transported to the lumen to power ATP synthesis by the ATP synthase. In the cyclic pathway (dotted blue line), electrons from PSI reenter the PQ pool. Thus, the cyclic pathway produces ATP at the expense of NADPH. Inhibitors used in this study and their sites of inhibition are also indicated in red octagons. DCMU blocks electron transfer from PSII to PQ and DBMIB prevents oxidation of plastoquinone by the cyt b6f complex. Cyt b6f, cytochrome b6 f complex; PC, plastocyanin; PQ, plastoquinone; PSI, photosystem I; PSII, photosystem II.« less

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Works referencing / citing this record:

Diverse hydrocarbon biosynthetic enzymes can substitute for olefin synthase in the cyanobacterium Synechococcus sp. PCC 7002
journal, February 2019


Modeling the Interplay between Photosynthesis, CO2 Fixation, and the Quinone Pool in a Purple Non-Sulfur Bacterium
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Improved lipid production via fatty acid biosynthesis and free fatty acid recycling in engineered Synechocystis sp. PCC 6803
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Diverse hydrocarbon biosynthetic enzymes can substitute for olefin synthase in the cyanobacterium Synechococcus sp. PCC 7002
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Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.