Rapid Transcriptional Reprogramming Triggered by Alteration of the Carbon/Nitrogen Balance Has an Impact on Energy Metabolism in Nostoc sp. PCC 7120.

Peter J. Gollan,Eva-Mari Aro,Dorota Muth-Pawlak

doi:10.3390/life10110297

Abstract

Nostoc (Anabaena) sp. PCC 7120 is a filamentous cyanobacterial species that fixes N2 to nitrogenous compounds using specialised heterocyst cells. Changes in the intracellular ratio of carbon to nitrogen (C/N balance) is known to trigger major transcriptional reprogramming of the cell, including initiating the differentiation of vegetative cells to heterocysts. Substantial transcriptional analysis has been performed on Nostoc sp. PCC 7120 during N stepdown (low to high C/N), but not during C stepdown (high to low C/N). In the current study, we shifted the metabolic balance of Nostoc sp. PCC 7120 cultures grown at 3% CO2 by introducing them to atmospheric conditions containing 0.04% CO2 for 1 h, after which the changes in gene expression were measured using RNAseq transcriptomics. This analysis revealed strong upregulation of carbon uptake, while nitrogen uptake and metabolism and early stages of heterocyst development were downregulated in response to the shift to low CO2. Furthermore, gene expression changes revealed a decrease in photosynthetic electron transport and increased photoprotection and reactive oxygen metabolism, as well a decrease in iron uptake and metabolism. Differential gene expression was largely attributed to change in the abundances of the metabolites 2-phosphoglycolate and 2-oxoglutarate, which signal a rapid shift from fluent photoassimilation to glycolytic metabolism of carbon after transition to low CO2. This work shows that the C/N balance in Nostoc sp. PCC 7120 rapidly adjusts the metabolic strategy through transcriptional reprogramming, enabling survival in the fluctuating environment.

Highlights

Cyanobacteria use light energy to fix inorganic carbon (Ci ) and nitrogen (N), harvested from their aquatic environment, into the metabolic components required for growth and propagation.Environmental sources of Ci include dissolved CO2 and bicarbonate (HCO3 − ), while N can be supplied by nitrate (NO3 − ), nitrite (NO2 − ), ammonium (NH4 + ), urea or N2
This study identified that genes encoding factors involved in photosynthetic electron transport, glycolysis and iron homeostasis are regulated by C/N homeostasis, which is suggested to trigger a transition from efficient photoautotrophic growth and energy storage to photoinhibition and glycolysis
PCC 7120 grown in BG11 under 3% CO2 -enriched air was compared with that of the same strain shifted from 3% CO2 to 0.04% CO2 for 1 h, revealing 230 genes to be upregulated >2-fold and 211 genes to be downregulated >2-fold, in the low CO2 condition

Summary

Introduction

Cyanobacteria use light energy to fix inorganic carbon (Ci ) and nitrogen (N), harvested from their aquatic environment, into the metabolic components required for growth and propagation.Environmental sources of Ci include dissolved CO2 and bicarbonate (HCO3 − ), while N can be supplied by nitrate (NO3 − ), nitrite (NO2 − ), ammonium (NH4 + ), urea or N2 (in diazotrophic cyanobacteria; reviewed in [1]). The tight coupling of the concentrations of Ci and N taken up from the environment prevents metabolic imbalance within the cell, which allows cyanobacteria to thrive amidst varying nutritional conditions. This is achieved in large part by transcriptional modifications that are triggered by fluctuations in the cellular homeostasis of organic carbon (C) and N, which are represented by changes in the relative abundances of key metabolite signals (reviewed in [2,3,4]).

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