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Title: The plasticity of cyanobacterial carbon metabolism

Abstract

This opinion article aims to raise awareness of a fundamental issue which governs sustainable production of biofuels and bio-chemicals from photosynthetic cyanobacteria. Discussed is the plasticity of carbon metabolism, by which the cyanobacterial cells flexibly distribute intracellular carbon fluxes towards target products and adapt to environmental/genetic alterations. This intrinsic feature in cyanobacterial metabolism is being understood through recent identification of new biochemical reactions and engineering on low-throughput pathways. We focus our discussion on new insights into the nature of metabolic plasticity in cyanobacteria and its impact on hydrocarbons (e.g. ethylene and isoprene) production. Here, we discuss approaches that need to be developed to rationally rewire photosynthetic carbon fluxes throughout primary metabolism. We also outline open questions about the regulatory mechanisms of the metabolic network that remain to be answered, which might shed light on photosynthetic carbon metabolism and help optimize design principles in order to improve the production of fuels and chemicals in cyanobacteria.

Authors:
 [1];  [1];  [1];  [1];  [1]
  1. National Renewable Energy Lab. (NREL), Golden, CO (United States)
Publication Date:
Research Org.:
National Renewable Energy Lab. (NREL), Golden, CO (United States)
Sponsoring Org.:
USDOE Office of Energy Efficiency and Renewable Energy (EERE), Bioenergy Technologies Office (EE-3B); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1399349
Report Number(s):
NREL/JA-2700-68379
Journal ID: ISSN 1367-5931
Grant/Contract Number:
AC36-08GO28308
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Current Opinion in Chemical Biology
Additional Journal Information:
Journal Volume: 41; Journal Issue: C; Journal ID: ISSN 1367-5931
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; biofuels; biochemicals; cyanobacteria

Citation Formats

Xiong, Wei, Cano, Melissa, Wang, Bo, Douchi, Damien, and Yu, Jianping. The plasticity of cyanobacterial carbon metabolism. United States: N. p., 2017. Web. doi:10.1016/j.cbpa.2017.09.004.
Xiong, Wei, Cano, Melissa, Wang, Bo, Douchi, Damien, & Yu, Jianping. The plasticity of cyanobacterial carbon metabolism. United States. doi:10.1016/j.cbpa.2017.09.004.
Xiong, Wei, Cano, Melissa, Wang, Bo, Douchi, Damien, and Yu, Jianping. 2017. "The plasticity of cyanobacterial carbon metabolism". United States. doi:10.1016/j.cbpa.2017.09.004.
@article{osti_1399349,
title = {The plasticity of cyanobacterial carbon metabolism},
author = {Xiong, Wei and Cano, Melissa and Wang, Bo and Douchi, Damien and Yu, Jianping},
abstractNote = {This opinion article aims to raise awareness of a fundamental issue which governs sustainable production of biofuels and bio-chemicals from photosynthetic cyanobacteria. Discussed is the plasticity of carbon metabolism, by which the cyanobacterial cells flexibly distribute intracellular carbon fluxes towards target products and adapt to environmental/genetic alterations. This intrinsic feature in cyanobacterial metabolism is being understood through recent identification of new biochemical reactions and engineering on low-throughput pathways. We focus our discussion on new insights into the nature of metabolic plasticity in cyanobacteria and its impact on hydrocarbons (e.g. ethylene and isoprene) production. Here, we discuss approaches that need to be developed to rationally rewire photosynthetic carbon fluxes throughout primary metabolism. We also outline open questions about the regulatory mechanisms of the metabolic network that remain to be answered, which might shed light on photosynthetic carbon metabolism and help optimize design principles in order to improve the production of fuels and chemicals in cyanobacteria.},
doi = {10.1016/j.cbpa.2017.09.004},
journal = {Current Opinion in Chemical Biology},
number = C,
volume = 41,
place = {United States},
year = 2017,
month = 9
}

Journal Article:
Free Publicly Available Full Text
This content will become publicly available on September 29, 2018
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  • Synechocystis sp. strain PCC 6803 has been widely used as a photo-biorefinery chassis. Based on its genome annotation, this species contains a complete TCA cycle, an Embden-Meyerhof-Parnas pathway (EMPP), an oxidative pentose phosphate pathway (OPPP), and an Entner–Doudoroff pathway (EDP). To evaluate how Synechocystis 6803 catabolizes glucose under heterotrophic conditions, we performed 13C metabolic flux analysis, metabolite pool size analysis, gene knockouts, and heterologous expressions. The results revealed a cyclic mode of flux through the OPPP. Small, but non-zero, fluxes were observed through the TCA cycle and the malic shunt. Independent knockouts of 6-phosphogluconate dehydrogenase (gnd) and malic enzyme (me)more » corroborated these results, as neither mutant could grow under dark heterotrophic conditions. Our data also indicate that Synechocystis 6803 metabolism relies upon oxidative phosphorylation to generate ATP from NADPH under dark or insufficient light conditions. The pool sizes of intermediates in the TCA cycle, particularly acetyl-CoA, were found to be several fold lower in Synechocystis 6803 (compared to E. coli metabolite pool sizes), while its sugar phosphate intermediates were several-fold higher. Moreover, negligible flux was detected through the native, or heterologous, EDP in the wild type or Δgnd strains under heterotrophic conditions. Comparing photoautotrophic, photomixotrophic, and heterotrophic conditions, the Calvin cycle, OPPP, and EMPP in Synechocystis 6803 possess the ability to regulate their fluxes under various growth conditions (plastic), whereas its TCA cycle always maintains at low levels (rigid). This work also demonstrates how genetic profiles do not always reflect actual metabolic flux through native or heterologous pathways. Biotechnol. Bioeng. 2017;114: 1593–1602. © 2017 Wiley Periodicals, Inc.« less
  • Hydrogen production by incubated cyanobacterial epiphytes occurred only in the dark, was stimulated by C/sub 2/H/sub 2/, and was inhibited by O/sub 2/. Addition of NO/sub 3//sup -/ inhibited dark, anaerobic H/sub 2/ production, whereas the addition of NH/sub 4//sup +/ inhibited N/sub 2/ fixation (C/sub 2/H/sub 2/ reduction) but not dark H/sub 2/ production. Aerobically incubated cyanobacterial aggregates consumed H/sub 2/, but light-incubated rates (3.6 mu mol of H/sub 2/ g-1 h-1) were statistically equivalent to dark uptake rates (4.8 mu mol of H/sub 2/ g-1 h-1), which were statistically equivalent to dark, anaerobic production rates (2.5 to 10more » mu mol of H/sub 2/ g-1 h-1). Production rates of H/sub 2/ were fourfold higher for aggregates in a more advanced stage of decomposition. Enrichment cultures of H/sub 2/-producing fermentative bacteria were recovered from freshly harvested, H/sub 2/-producing cyanobacterial aggregates. Hydrogen production in these cyanobacterial communities appears to be caused by the resident bacterial flora and not by the cyanobacteria. In situ areal estimates of dark H/sub 2/ production by submerged epiphytes (6.8 mu mol of H/sub 2/ m-2 h-1) were much lower than rates of light-driven N/sub 2/ fixation by the epiphytic cyanobacteria (310 mu mol of C/sub 2/H/sub 4/ meters -2 h-1). (26 Refs.)« less