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:
-
- Washington Univ., St. Louis, MO (United States). Dept. of Energy, Environmental, and Chemical Engineering
- Washington Univ., St. Louis, MO (United States). Dept. of Biology; Pennsylvania State Univ., University Park, PA (United States). Dept. of Chemical Engineering
- Pennsylvania State Univ., University Park, PA (United States). Dept. of Chemical Engineering
- 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}
}
Figures / Tables:
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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
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Figures / Tables found in this record: