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Trade-off between growth and carbohydrate accumulation in nutrient-limited Arthrospira sp. PCC 8005 studied by integrating transcriptomic and proteomic approaches

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%). 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.

ORGANISM(S): Limnospira indica PCC 8005

PROVIDER: GSE67839 | GEO | 2016/04/20

SECONDARY ACCESSION(S): PRJNA281049

REPOSITORIES: GEO

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Project description:Metabolic flexibility in aerobic methane oxidising bacteria (methanotrophs) enhances cell growth and survival in instances where resources are variable or limiting. Examples include the production of intracellular compounds (such as glycogen or polyhydroxyalkanoates) in response to unbalanced growth conditions and the use of some energy substrates, besides methane, when available. Indeed, recent studies show that verrucomicrobial methanotrophs can grow mixotrophically through oxidation of hydrogen and methane gases via respiratory membrane-bound group 1d [NiFe] hydrogenases and methane monooxygenases respectively. Hydrogen metabolism is particularly important for adaptation to methane and oxygen limitation, suggesting this metabolic flexibility may confer growth and survival advantages. In this work, we provide evidence that, in adopting a mixotrophic growth strategy, the thermoacidophilic methanotroph, Methylacidiphilum sp. RTK17.1 changes its growth rate, biomass yields and the production of intracellular glycogen reservoirs. Under nitrogen-fixing conditions, removal of hydrogen from the feed-gas resulted in a 14 % reduction in observed growth rates and a 144% increase in cellular glycogen content. Concomitant with increases in glycogen content, the total protein content of biomass decreased following the removal of hydrogen. Transcriptome analysis of Methylacidiphilum sp. RTK17.1 revealed a 3.5-fold upregulation of the Group 1d [NiFe] hydrogenase in response to oxygen limitation and a 4-fold upregulation of nitrogenase encoding genes (nifHDKENX) in response to nitrogen limitation. Genes associated with glycogen synthesis and degradation were expressed constitutively and did not display evidence of transcriptional regulation. Collectively these data further challenge the belief that hydrogen metabolism in methanotrophic bacteria is primarily associated with energy conservation during nitrogen fixation and suggests its utilisation provides a competitive growth advantage within hypoxic habitats.

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Trade-off between growth and carbohydrate accumulation in nutrient-limited Arthrospira sp. PCC 8005 studied by integrating transcriptomic and proteomic approaches

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