Trade-Off between Growth and Carbohydrate Accumulation in Nutrient-Limited Arthrospira sp. PCC 8005 Studied by Integrating Transcriptomic and Proteomic Approaches.

Orily Depraetere,Hanène Badri,Imogen Foubert,Ruddy Wattiez,Natalie Leys,Frédéric Deschoenmaeker,Pieter Monsieurs,Koenraad Muylaert,Douglas Andrew Campbell

doi:10.1371/journal.pone.0132461

Abstract

Cyanobacteria have a strong potential for biofuel production due to their ability to accumulate large amounts of carbohydrates. Nitrogen (N) stress can be used to increase the content of carbohydrates in the biomass, but it is expected to reduce biomass productivity. To study this trade-off between carbohydrate accumulation and biomass productivity, we characterized the biomass productivity, biomass composition as well as the transcriptome and proteome of the cyanobacterium Arthrospira sp. PCC 8005 cultured under N-limiting and N-replete conditions. N limitation resulted in a large increase in the carbohydrate content of the biomass (from 14 to 74%) and a decrease in the protein content (from 37 to 10%). Analyses of fatty acids indicated that no lipids were accumulated under N-limited conditions. Nevertheless, it did not affect the biomass productivity of the culture up to five days after N was depleted from the culture medium. Transcriptomic and proteomic analysis indicated that de novo protein synthesis was down-regulated in the N-limited culture. Proteins were degraded and partly converted into carbohydrates through gluconeogenesis. Cellular N derived from protein degradation was recycled through the TCA and GS-GOGAT cycles. In addition, photosynthetic energy production and carbon fixation were both down-regulated, while glycogen synthesis was up-regulated. Our results suggested that N limitation resulted in a redirection of photosynthetic energy from protein synthesis to glycogen synthesis. The fact that glycogen synthesis has a lower energy demand than protein synthesis might explain why Arthrospira is able to achieve a similar biomass productivity under N-limited as under N-replete conditions despite the fact that photosynthetic energy production was impaired by N limitation.

Highlights

Microalgae are considered to be a promising feedstock for the production of biofuels [1,2]
Carbohydrates can be converted into bio-ethanol using alcoholic fermentation or into bio-methane using anaerobic digestion [3]. This carbohydrate route for biofuel production is more efficient in terms of light energy conversion into bio-energy feedstocks than the classical biodiesel route [4]
6.3 moles ATP per C are required for the production of lipids in microalgae as opposed to only 4.2 ATP per C for carbohydrates, which corresponds to a 50% higher energy demand

Summary

Introduction

Microalgae are considered to be a promising feedstock for the production of biofuels [1,2]. Carbohydrates can be converted into bio-ethanol using alcoholic fermentation or into bio-methane using anaerobic digestion [3]. This carbohydrate route for biofuel production is more efficient in terms of light energy conversion into bio-energy feedstocks than the classical biodiesel route [4]. 6.3 moles ATP per C are required for the production of lipids in microalgae as opposed to only 4.2 ATP per C for carbohydrates (i.e., a difference of 53%), which corresponds to a 50% higher energy demand. Lipids only yield 41% more energy than carbohydrates in thermal oxidation processes (i.e., as biodiesel), and only 32% more in biochemical oxidation (i.e., in bio-methane or bio-ethanol formation) [4]

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Conclusion