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

Bertram M Berla,Himadri B Pakrasi,Rajib Saha,Costas D Maranas

doi:10.1038/srep14894

Bertram M Berla, Himadri B Pakrasi + Show 2 more

Open Access

https://doi.org/10.1038/srep14894

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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.

Highlights

Biofuel highlights the gap that still exists between the dream of a plug-and-play microbial cell factory and the reality of a dynamically regulated, intricately interconnected, and poorly understood cellular environment
We argue that alkanes are critical metabolites at low temperature because they help to maintain the balance of photosynthetic activities in the thylakoid membrane
At low temperatures, alkanes modulate reductant partitioning and their absence leads to increased reliance on cyclic electron flow (CEF)

Summary

Introduction

Biofuel highlights the gap that still exists between the dream of a plug-and-play microbial cell factory and the reality of a dynamically regulated, intricately interconnected, and poorly understood cellular environment. The cyanobacterial thylakoid membrane is unique because it houses both an oxygen-evolving photosynthetic apparatus and a full complement of respiratory enzymes[15,16,17] This diversity of functions poses both a challenge and an opportunity: it allows these organisms to adapt to a wide range of conditions and maintain balance among diverse metabolic pathways. It has been suggested that cyclic electron transport pathways are critical for achieving the appropriate balance of ATP and NADPH to power CO2 fixation[25,26,28] These electron transport pathways must power other cellular processes such as nitrogen assimilation, macromolecule synthesis, and the carbon-concentrating mechanism. Because of its prominent role as a model system for photosynthesis studies, much more is known about such pathways in Synechocystis 6803 as compared with any other cyanobacterium

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