Cyanobacterial carbon metabolism: Fluxome plasticity and oxygen dependence

Biotechnology and Bioengineering

Volumn 114, Issue 7, 2017, Pages 1593-1602

  Wan, Ni ^a   DeLorenzo, Drew M ^a   He, Lian ^a   You, Le ^a   Immethun, Cheryl M ^a   Wang, George ^b,c   Baidoo, Edward E K ^b,c   Hollinshead, Whitney ^a   Keasling, Jay D ^b,c,d,e,f,g   Moon, Tae Seok ^a   Tang, Yinjie J ^a  

^a WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

^b Joint Bioenergy Institute   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e University of California at Berkeley   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g Chalmers University of Technology   (Denmark)

Author keywords

13C metabolic flux analysis; metabolite pool size; oxidative pentose phosphate pathway; TCA

Indexed keywords

BIOMOLECULES; CARBON; ESCHERICHIA COLI; GENE EXPRESSION; LAKES; METABOLITES; PHYSIOLOGY; SUGARS;

6-PHOSPHOGLUCONATE DEHYDROGENASE; ENTNER DOUDOROFF PATHWAYS; HETEROLOGOUS EXPRESSION; HETEROTROPHIC CONDITIONS; METABOLIC FLUX ANALYSIS; METABOLITE POOLS; OXIDATIVE PENTOSE PHOSPHATE PATHWAYS; OXIDATIVE PHOSPHORYLATION;

METABOLISM;

ACETYL COENZYME A; ADENOSINE TRIPHOSPHATE; MALATE DEHYDROGENASE (DECARBOXYLATING); OXYGEN; PHOSPHOGLUCONATE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; BACTERIAL PROTEIN; CARBON; PROTEOME;

ARTICLE; BACTERIAL GROWTH; BACTERIAL METABOLISM; CARBON DIOXIDE FIXATION; CARBON METABOLISM; CITRIC ACID CYCLE; GENE INACTIVATION; GLUCOSE TRANSPORT; GLYCOLYSIS; GROWTH RATE; HOMOLOGOUS RECOMBINATION; METABOLIC FLUX ANALYSIS; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PENTOSE PHOSPHATE CYCLE; PHOTOSYNTHESIS; SIGNAL TRANSDUCTION; SYNECHOCYSTIS SP. PCC 6803; CELL PLASTICITY; METABOLISM; METABOLOME; OXYGEN CONSUMPTION; PHYSIOLOGY; PROCEDURES; SYNECHOCYSTIS;

BACTERIAL PROTEINS; CARBON; CELL PLASTICITY; METABOLIC FLUX ANALYSIS; METABOLOME; OXYGEN; OXYGEN CONSUMPTION; PROTEOME; SYNECHOCYSTIS;

EID: 85016712850     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.26287     Document Type: Article

References (43)

1. Allan Wendy L, Clark Shawn M, Hoover Gordon J, Shelp Barry J. 2009. Role of plant glyoxylate reductases during stress: A hypothesis. Biochem J 423(Pt 1):15–22.
2. Anderson S, McIntosh L. 1991. Light-activated heterotrophic growth of the cyanobacterium Synechocystis sp. strain PCC 6803: A blue-light-requiring process. J Bacteriol 173:2761–2767.
3. Angermayr SA, Rovira AG, Hellingwerf KJ. 2015. Metabolic engineering of cyanobacteria for the synthesis of commodity products. Trends Biotechnol 33(6):352–361.
4. Antoniewicz MR, Kelleher JK, Stephanopoulos G. 2007. Accurate assessment of amino acid mass isotopomer distributions for metabolic flux analysis. Anal Chem 79(19):7554–7559.
5. Bar-Even A, Flamholz A, Noor E, Milo R. 2012. Rethinking glycolysis: On the biochemical logic of metabolic pathways. Nat Chem Biol 8(6):509–517.
6. Bar-Even A, Noor E, Flamholz A, Milo R. 2013. Design and analysis of metabolic pathways supporting formatotrophic growth for electricity-dependent cultivation of microbes. Biochimica et Biophysica Acta (BBA) − Bioenergetics 1827(8-9):1039–1047.
7. Bennett BD, Yuan J, Kimball EH, Rabinowitz JD. 2008. Absolute quantitation of intracellular metabolite concentrations by an isotope ratio-based approach. Nat Protoc 3(8):1299–1311.
8. Berla BM, Saha R, Immethun CM, Maranas CD, Moon TS, Pakrasi HB. 2013. Synthetic biology of cyanobacteria: Unique challenges and opportunities. Front Microbiol 4:246.
9. Bogorad I, Lin T-S, Liao J. 2013. Synthetic non-oxidative glycolysis enables complete carbon conservation. Nature 502:693–697.
10. Bricker TM, Zhang S, Laborde SM, Mayer PR, Frankel LK, Moroney JV. 2004. The malic enzyme is required for optimal photoautotrophic growth of Synechocystis sp. strain PCC 6803 under continuous light but not under a diurnal light regimen. J Bacteriol 186(23):8144–8148.
11. Brown DJ. 2009. The chemistry of heterocyclic compounds. The Pyrimidines. Hoboken, NJ: John Wiley & Sons.
12. Chen X, Schreiber K, Appel J, Makowka A, Fähnrich B, Roettger M, Hajirezaei MR, Sönnichsen FD, Schönheit P, Martin WF, Gutekunst K. 2016. The Entner–Doudoroff pathway is an overlooked glycolytic route in cyanobacteria and plants. Proc Natl Acad Sci USA 113(19):5441–5446.
13. Dauner M, Bailey JE, Sauer U. 2001. Metabolic flux analysis with a comprehensive isotopomer model in Bacillus subtilis. Biotechnol Bioeng 76(2):144–156.
14. Ducat DC, Way JC, Silver PA. 2011. Engineering cyanobacteria to generate high-value products. Trends Biotechnol 29(2):95–103.
15. 13C-metabolite fingerprinting. Biotechnol Bioeng 113(1):91–100.
16. Immethun CM, Ng KM, DeLorenzo DM, Waldron-Feinstein B, Lee Y-C, Moon TS. 2016. Oxygen-responsive genetic circuits constructed in Synechocystis sp. PCC 6803. Biotechnol Bioeng 113(2):433–442.
17. Lee HW, Oh CH, Geyer A, Pfleiderer W, Park YS. 1999. Characterization of a novel unconjugated pteridine glycoside, cyanopterin, in Synechocystis sp. PCC 6803. Biochimica et Biophysica Acta (BBA)-Bioenergetics 1410(1):61–70.
18. 13C-labeled extracts. A new method for accurate quantification of changes in concentrations of intracellular metabolites. Biotechnol Bioeng 85(6):620–628.
19. Mohammadi R, Fallah-Mehrabadi J, Bidkhori G, Zahiri J, Javad Niroomand M, Masoudi-Nejad A. 2016. A systems biology approach to reconcile metabolic network models with application to Synechocystis sp. PCC 6803 for biofuel production. Mol BioSyst 12(8):2552–2561.
20. Montagud A, Navarro E, Fernandez de Cordoba P, Urchueguia J, Patil K. 2010. Reconstruction and analysis of genome-scale metabolic model of a photosynthetic bacterium. BMC Syst Biol 4(1):156–171.
21. Mrázek J, Bhaya D, Grossman AR, Karlin S. 2001. Highly expressed and alien genes of the Synechocystis genome. Nucleic Acids Res 29(7):1590–1601.
22. Nakajima T, Kajihata S, Yoshikawa K, Matsuda F, Furusawa C, Hirasawa T, Shimizu H. 2014. Integrated metabolic flux and omics analysis of synechocystis sp. PCC 6803 under mixotrophic and photoheterotrophic conditions. Plant Cell Physiol 55(9):1605–1612.
23. Nogales J, Gudmundsson S, Knight EM, Palsson BO, Thiele I. 2012. Detailing the optimality of photosynthesis in cyanobacteria through systems biology analysis. Proc Natl Acad Sci USA 109(7):2678–2683.
24. Richardson LL, Castenholz RW. 1987. Enhanced survival of the cyanobacterium Oscillatoria terebriformis in darkness under anaerobic conditions. Appl Environ Microbiol 53(9):2151–2158.
25. Saha R, Liu D, Hoynes-O'Connor A, Liberton M, Yu J, Bhattacharyya-Pakrasi M, Balassy A, Zhang F, Moon TS, Maranas CD, Pakrasi HB. 2016. Diurnal regulation of cellular processes in the cyanobacterium synechocystis sp. strain PCC 6803: Insights from transcriptomic, fluxomic, and physiological analyses. mBio 7(3):e00464–e00416.
26. Shastri A, Morgan J. 2005. Flux balance analysis of photoautotrophic metabolism. Biotechnol Prog 21:1617–1626.
27. Sweetlove LJ, Beard KFM, Nunes-Nesi A, Fernie AR, Ratcliffe RG. 2010. Not just a circle: Flux modes in the plant TCA cycle. Trends Plant Sci 15(8):462–470.
28. Tabei Y, Okada K, Tsuzuki M. 2007. Sll1330 controls the expression of glycolytic genes in Synechocystis sp. PCC 6803. Biochem Biophys Res Commun 355(4):1045–1050.
29. Tai Y-S, Xiong M, Jambunathan P, Wang J, Wang J, Stapleton C, Zhang K. 2016. Engineering nonphosphorylative metabolism to generate lignocellulose-derived products. Nat Chem Biol 12(4):247–253.
30. Tamoi M, Miyazaki T, Fukamizo T, Shigeoka S. 2005. The Calvin cycle in cyanobacteria is regulated by CP12 via the NAD(H)/NADP(H) ratio under light/dark conditions. Plant J 42(4):504–513.
31. Vemuri G, Altman E, Sangurdekar D, Khodursky A, Eiteman M. 2006. Overflow metabolism in Escherichia coli during steady-state growth: Transcriptional regulation and effect of the redox ratio. Appl Environ Microbiol 72(5):3653–3661.
32. 13C flux analysis: Mass isotope correction, data consistency checking, and precursor relationships. Biotechnol Bioeng 85(3):259–268.
33. Wan N, Abernathy M, JK-H Tang, Tang YJ, You L. 2015. Cyanobacterial photo-driven mixotrophic metabolism and its advantages for biosynthesis. Front Chem Sci Eng 9(3):308–316.
34. Xiong W, Brune D, Vermaas WF. 2014. The γ-aminobutyric acid shunt contributes to closing the tricarboxylic acid cycle in Synechocystis sp. PCC 6803. Mol Microbiol 93(4):786–796.
35. Xiong W, Lee T-C, Rommelfanger S, Gjersing E, Cano M, Maness P-C, Ghirardi M, Yu J. 2015a. Phosphoketolase pathway contributes to carbon metabolism in cyanobacteria. Nat Plants 2:15187.
36. 2 conversion to ethylene. Nat Plants 1(5).
37. 13C-labeled glucose. Metab Eng. 4(3):202–216.
38. Yoshikawa K, Hirasawa T, Shimizu H. 2015. Effect of malic enzyme on ethanol production by Synechocystis sp. PCC 6803. J Biosci Bioeng 119(1):82–84.
39. 13C-MFA delineates the photomixotrophic metabolism of Synechocystis sp. PCC 6803 under light- and carbon-sufficient conditions. Biotechnol J 9(5):684–692.
40. You L, He L, Tang YJ. 2015. Photoheterotrophic fluxome in Synechocystis sp. PCC 6803 and its implications for cyanobacterial bioenergetics. J Bacteriol 197(5):943–950.
41. 13C-labeling of proteinogenic amino acids. J Vis Exp 26(59):e3583.
42. 13C flux analysis. Metab Eng 13(6):656–665.
43. Yu Y, You L, Liu D, Hollinshead W, Tang YJ, Zhang F. 2013. Development of Synechocystis sp. PCC 6803 as a phototrophic cell factory. Mar Drugs 11(8):2894–2916.