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Reconstruction of a regulated two-cell metabolic model to study biohydrogen production in a diazotrophic cyanobacterium Anabaena variabilis ATCC 29413


Autoři: Ali Malek Shahkouhi aff001;  Ehsan Motamedian aff001
Působiště autorů: Department of Biotechnology, Faculty of Chemical Engineering, Tarbiat Modares University, Tehran, Iran aff001
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0227977

Souhrn

Anabaena variabilis is a diazotrophic filamentous cyanobacterium that differentiates to heterocysts and produces hydrogen as a byproduct. Study on metabolic interactions of the two differentiated cells provides a better understanding of its metabolism especially for improving hydrogen production. To this end, a genome-scale metabolic model for Anabaena variabilis ATCC 29413, iAM957, was reconstructed and evaluated in this research. Then, the model and transcriptomic data of the vegetative and heterocyst cells were applied to construct a regulated two-cell metabolic model. The regulated model improved prediction for biomass in high radiation levels. The regulated model predicts that heterocysts provide an oxygen-free environment and then, this model was used to find strategies for improving hydrogen production in heterocysts. The predictions indicate that the removal of uptake hydrogenase improves hydrogen production which is consistent with previous empirical research. Furthermore, the regulated model proposed activation of some reactions to provide redox cofactors which are required for improving hydrogen production up to 60% by bidirectional hydrogenase.

Klíčová slova:

Anabaena – Cell metabolism – Cyanobacteria – Hydrogen – Nitrogen metabolism – Oxygen – Oxygen metabolism – Photons


Zdroje

1. Buick R. When did oxygenic photosynthesis evolve? Philosophical Transactions of the Royal Society B: Biological Sciences. 2008;363(1504):2731–43. doi: 10.1098/rstb.2008.0041 18468984

2. Shevela D, Pishchalnikov RY. Oxygenic photosynthesis in cyanobacteria: CRC Press Boca Raton; 2013.

3. Vincent WF, Quesada A. Cyanobacteria in high latitude lakes, rivers and seas. Ecology of cyanobacteria II: Springer; 2012. p. 371–85.

4. Erdrich P, Knoop H, Steuer R, Klamt S. Cyanobacterial biofuels: new insights and strain design strategies revealed by computational modeling. Microbial Cell Factories. 2014;13(1):128.

5. Beck C, Knoop H, Axmann IM, Steuer R. The diversity of cyanobacterial metabolism: genome analysis of multiple phototrophic microorganisms. BMC genomics. 2012;13(1):56.

6. Berla BM, Saha R, Immethun CM, Maranas CD, Moon TS, Pakrasi H. Synthetic biology of cyanobacteria: unique challenges and opportunities. Frontiers in microbiology. 2013;4:246. doi: 10.3389/fmicb.2013.00246 24009604

7. Steuer R, Knoop H, Machné R. Modelling cyanobacteria: from metabolism to integrative models of phototrophic growth. Journal of experimental botany. 2012;63(6):2259–74. doi: 10.1093/jxb/ers018 22450165

8. Nogales J, Gudmundsson S, Thiele I. Toward systems metabolic engineering in cyanobacteria: opportunities and bottlenecks. Bioengineered. 2013;4(3):158–63. doi: 10.4161/bioe.22792 23138691

9. Burnap RL. Systems and photosystems: cellular limits of autotrophic productivity in cyanobacteria. Frontiers in bioengineering and biotechnology. 2015;3:1. doi: 10.3389/fbioe.2015.00001 25654078

10. Quintana N, Van der Kooy F, Van de Rhee MD, Voshol GP, Verpoorte R. Renewable energy from Cyanobacteria: energy production optimization by metabolic pathway engineering. Applied microbiology and biotechnology. 2011;91(3):471–90. doi: 10.1007/s00253-011-3394-0 21691792

11. Machado IM, Atsumi S. Cyanobacterial biofuel production. Journal of biotechnology. 2012;162(1):50–6. doi: 10.1016/j.jbiotec.2012.03.005 22446641

12. Ducat DC, Way JC, Silver PA. Engineering cyanobacteria to generate high-value products. Trends in biotechnology. 2011;29(2):95–103. doi: 10.1016/j.tibtech.2010.12.003 21211860

13. Rosgaard L, de Porcellinis AJ, Jacobsen JH, Frigaard N-U, Sakuragi Y. Bioengineering of carbon fixation, biofuels, and biochemicals in cyanobacteria and plants. Journal of biotechnology. 2012;162(1):134–47. doi: 10.1016/j.jbiotec.2012.05.006 22677697

14. Torres-Sánchez A, Gómez-Gardeñes J, Falo F. An integrative approach for modeling and simulation of heterocyst pattern formation in cyanobacteria filaments. PLoS computational biology. 2015;11(3):e1004129. doi: 10.1371/journal.pcbi.1004129 25816286

15. Perez R, Forchhammer K, Salerno G, Maldener I. Clear differences in metabolic and morphological adaptations of akinetes of two Nostocales living in different habitats. Microbiology. 2016;162(2):214–23. doi: 10.1099/mic.0.000230 26679176

16. Kumar K, Mella-Herrera RA, Golden JW. Cyanobacterial heterocysts. Cold Spring Harb Perspect Biol. 2009;2.

17. Stanier R, Bazine G. Phototrophic prokaryotes: the cyanobacteria. Annual Reviews in Microbiology. 1977;31(1):225–74.

18. Peter Wolk C. Heterocyst formation. Annual review of genetics. 1996;30(1):59–78.

19. Flores E, Herrero A. Compartmentalized function through cell differentiation in filamentous cyanobacteria. Nat Rev Microbiol. 2010;8.

20. Gerdtzen ZP, Salgado JC, Osses A, Asenjo JA, Rapaport I, Andrews BA, editors. Modeling heterocyst pattern formation in cyanobacteria. BMC bioinformatics; 2009: BioMed Central.

21. Herrero A, Picossi S, Flores E. Gene expression during heterocyst differentiation. Advances in botanical research. 65: Elsevier; 2013. p. 281–329.

22. Adams DG. Heterocyst formation in cyanobacteria. Current opinion in microbiology. 2000;3(6):618–24. doi: 10.1016/s1369-5274(00)00150-8 11121783

23. Wolk CP, Ernst A, Elhai J. Heterocyst metabolism and development. In: Bryant DA, editor. The Molecular Biology of Cyanobacteria. Dordrecht: Kluwer Academic Publishers; 1994.

24. Fay P. Oxygen relations of nitrogen fixation in cyanobacteria. Microbiological reviews. 1992;56(2):340–73. 1620069

25. Donze M, Haveman J, Schiereck P. Absence of photosystem 2 in heterocysts of blue-green alga Anabaena. Biochim Biophys Acta. 1972;256.

26. Curatti L, Flores E, Salerno G. Sucrose is involved in the diazotrophic metabolism of the heterocyst-forming cyanobacterium Anabaena sp. FEBS Lett. 2002;513.

27. Kolman MA, Nishi CN, Perez-Cenci M, Salerno GL. Sucrose in cyanobacteria: from a salt-response molecule to play a key role in nitrogen fixation. Life. 2015;5(1):102–26. doi: 10.3390/life5010102 25569239

28. Meeks JC, Elhai J. Regulation of cellular differentiation in filamentous cyanobacteria in free-living and plant-associated symbiotic growth states. Microbiology and Molecular Biology Reviews. 2002;66(1):94–121. doi: 10.1128/MMBR.66.1.94-121.2002 11875129

29. Henry CS, DeJongh M, Best AA, Frybarger PM, Linsay B, Stevens RL. High-throughput generation, optimization and analysis of genome-scale metabolic models. Nature biotechnology. 2010;28(9):977. doi: 10.1038/nbt.1672 20802497

30. Orth JD, Thiele I, Palsson BØ. What is flux balance analysis? Nature biotechnology. 2010;28(3):245–8. doi: 10.1038/nbt.1614 20212490

31. Price ND, Reed JL, Palsson BØ. Genome-scale models of microbial cells: evaluating the consequences of constraints. Nature Reviews Microbiology. 2004;2(11):886. doi: 10.1038/nrmicro1023 15494745

32. Shastri AA, Morgan JA. Flux balance analysis of photoautotrophic metabolism. Biotechnology progress. 2005;21(6):1617–26. doi: 10.1021/bp050246d 16321043

33. Nogales J, Gudmundsson S, Knight EM, Palsson BO, Thiele I. Detailing the optimality of photosynthesis in cyanobacteria through systems biology analysis. Proceedings of the National Academy of Sciences. 2012;109(7):2678–83.

34. Knoop H, Gründel M, Zilliges Y, Lehmann R, Hoffmann S, Lockau W, et al. Flux balance analysis of cyanobacterial metabolism: the metabolic network of Synechocystis sp. PCC 6803. PLoS Comput Biol. 2013;9(6):e1003081. doi: 10.1371/journal.pcbi.1003081 23843751

35. Saha R, Verseput AT, Berla BM, Mueller TJ, Pakrasi HB, Maranas CD. Reconstruction and comparison of the metabolic potential of cyanobacteria Cyanothece sp. ATCC 51142 and Synechocystis sp. PCC 6803. PloS one. 2012;7(10):e48285. doi: 10.1371/journal.pone.0048285 23133581

36. Malatinszky D, Steuer R, Jones PR. A comprehensively curated genome-scale two-cell model for the heterocystous cyanobacterium Anabaena sp. PCC 7120. Plant physiology. 2017;173(1):509–23. doi: 10.1104/pp.16.01487 27899536

37. Salleh SF, Kamaruddin A, Uzir MH, Mohamed AR. Effects of cell density, carbon dioxide and molybdenum concentration on biohydrogen production by Anabaena variabilis ATCC 29413. Energy Conversion and Management. 2014;87:599–605.

38. Weyman PD, Pratte B, Thiel T. Hydrogen production in nitrogenase mutants in Anabaena variabilis. FEMS microbiology letters. 2010;304(1):55–61. doi: 10.1111/j.1574-6968.2009.01883.x 20070369

39. Tsygankov A, Serebryakova L, Sveshnikov D, Rao K, Gogotov I, Hall D. Hydrogen photoproduction by three different nitrogenases in whole cells of Anabaena variabilis and the dependence on pH. International journal of hydrogen energy. 1997;22(9):859–67.

40. Tiwari A, Pandey A. Cyanobacterial hydrogen production–a step towards clean environment. International journal of hydrogen energy. 2012;37(1):139–50.

41. Dutta D, De D, Chaudhuri S, Bhattacharya SK. Hydrogen production by cyanobacteria. Microbial Cell Factories. 2005;4(1):1.

42. Park J-J, Lechno-Yossef S, Wolk CP, Vieille C. Cell-specific gene expression in Anabaena variabilis grown phototrophically, mixotrophically, and heterotrophically. BMC genomics. 2013;14(1):759.

43. Motamedian E, Mohammadi M, Shojaosadati SA, Heydari M. TRFBA: an algorithm to integrate genome-scale metabolic and transcriptional regulatory networks with incorporation of expression data. Bioinformatics. 2016;33(7):1057–63.

44. Khetkorn W, Baebprasert W, Lindblad P, Incharoensakdi A. Redirecting the electron flow towards the nitrogenase and bidirectional Hox-hydrogenase by using specific inhibitors results in enhanced H2 production in the cyanobacterium Anabaena siamensis TISTR 8012. Bioresource technology. 2012;118:265–71. doi: 10.1016/j.biortech.2012.05.052 22705533

45. Thiele I, Palsson BØ. A protocol for generating a high-quality genome-scale metabolic reconstruction. Nature protocols. 2010;5(1):93–121. doi: 10.1038/nprot.2009.203 20057383

46. Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic acids research. 2000;28(1):27–30. doi: 10.1093/nar/28.1.27 10592173

47. Caspi R, Billington R, Ferrer L, Foerster H, Fulcher CA, Keseler IM, et al. The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic acids research. 2016;44(D1):D471–D80. doi: 10.1093/nar/gkv1164 26527732

48. Nakao M, Okamoto S, Kohara M, Fujishiro T, Fujisawa T, Sato S, et al. CyanoBase: the cyanobacteria genome database update 2010. Nucleic acids research. 2009:gkp915.

49. King ZA, Lu J, Dräger A, Miller P, Federowicz S, Lerman JA, et al. BiGG Models: A platform for integrating, standardizing and sharing genome-scale models. Nucleic acids research. 2016;44(D1):D515–D22. doi: 10.1093/nar/gkv1049 26476456

50. Chang A, Schomburg I, Placzek S, Jeske L, Ulbrich M, Xiao M, et al. BRENDA in 2015: exciting developments in its 25th year of existence. Nucleic acids research. 2014:gku1068.

51. Consortium U. UniProt: a hub for protein information. Nucleic acids research. 2014:gku989.

52. Schellenberger J, Que R, Fleming RM, Thiele I, Orth JD, Feist AM, et al. Quantitative prediction of cellular metabolism with constraint-based models: the COBRA Toolbox v2. 0. Nature protocols. 2011;6(9):1290–307. doi: 10.1038/nprot.2011.308 21886097

53. Vargas M, Rodriguez H, Moreno J, Olivares H, Del Campo J, Rivas J, et al. Biochemical composition and fatty acid content of filamentous nitrogen-fixing cyanobacteria. Journal of phycology. 1998;34(5):812–7.

54. Naoki S, Norio M, Yoshiro M, Nobuo U. Effect of growth temperature on lipid and fatty acid compositions in the blue-green algae, Anabaena variabilis and Anacystis nidulans. Biochimica et Biophysica Acta (BBA)-Lipids and Lipid Metabolism. 1979;572(1):19–28.

55. Ernst A, Kirschenlohr H, Diez J, Böger P. Glycogen content and nitrogenase activity in Anabaena variabilis. Archives of Microbiology. 1984;140(2–3):120–5.

56. Rodriguez H, Rivas J, Guerrero MG, Losada M. Nitrogen-fixing cyanobacterium with a high phycoerythrin content. Applied and environmental microbiology. 1989;55(3):758–60. 16347884

57. Healey F. THE CAROTENOIDS OF FOUR BLUE-GREEN ALGAE1. Journal of phycology. 1968;4(2):126–9. doi: 10.1111/j.1529-8817.1968.tb04685.x 27067947

58. Stocker A, Woggon WD, Rüttimann A. Identification of The Tocopherol-Cyclase in the Blue-Green Algae Anabaena variabilis KÜTZING (Cyanobacteria). Helvetica chimica acta. 1993;76(4):1729–38.

59. Rai AN, Rowell P, Stewart WD. Glutamate Synthase Activity of Heterocysts and Vegetative Cells of the Cyanobacterium Anabaena variabilis Kütz. Microbiology. 1982;128(9):2203–5.

60. Martín-Figueroa E, Navarro F, Florencio FJ. The GS-GOGAT pathway is not operative in the heterocysts. Cloning and expression of glsF gene from the cyanobacterium Anabaena sp. PCC 7120. FEBS Lett. 2000;476.

61. Thomas J, Meeks JC, Wolk CP, Shaffer PW, Austin SM. Formation of glutamine from 13N-ammonia, 13N-dinitrogen, and 14C-glutamate by heterocysts isolated from Anabaena cylindrica. J Bacteriol. 1977;129.

62. Mariscal V, Herrero A, Flores E. Continuous periplasm in a filamentous, heterocyst-forming cyanobacterium. Molecular microbiology. 2007;65(4):1139–45. doi: 10.1111/j.1365-2958.2007.05856.x 17645442

63. Berberoğlu H, Barra N, Pilon L, Jay J. Growth, CO₂ consumption and H₂ production of Anabaena variabilis ATCC 29413-U under different irradiances and CO₂ concentrations. Journal of applied microbiology. 2008.

64. Salleh SF, Kamaruddin A, Uzir MH, Karim KA, Mohamed AR. Investigation of the links between heterocyst and biohydrogen production by diazotrophic cyanobacterium A. variabilis ATCC 29413. Archives of microbiology. 2016;198(2):101–13. doi: 10.1007/s00203-015-1164-6 26521065

65. Berberoğlu H, Jay J, Pilon L. Effect of nutrient media on photobiological hydrogen production by Anabaena variabilis ATCC 29413. International Journal of Hydrogen Energy. 2008;33(4):1172–84.

66. Yoon JH, Sim SJ, Kim M-S, Park TH. High cell density culture of Anabaena variabilis using repeated injections of carbon dioxide for the production of hydrogen. International journal of hydrogen energy. 2002;27(11–12):1265–70.

67. Yoon JH, Shin J-H, Park TH. Characterization of factors influencing the growth of Anabaena variabilis in a bubble column reactor. Bioresource technology. 2008;99(5):1204–10. doi: 10.1016/j.biortech.2007.02.012 17383870

68. Agel G, Nultsch W, Rhiel E. Photoinhibition and its wavelength dependence in the cyanobacterium Anabaena variabilis. Archives of Microbiology. 1987;147(4):370–4.

69. Markou G, Georgakakis D. Cultivation of filamentous cyanobacteria (blue-green algae) in agro-industrial wastes and wastewaters: a review. Applied Energy. 2011;88(10):3389–401.

70. Mahadevan R, Schilling C. The effects of alternate optimal solutions in constraint-based genome-scale metabolic models. Metabolic engineering. 2003;5(4):264–76. doi: 10.1016/j.ymben.2003.09.002 14642354

71. Nürnberg DJ, Mariscal V, Bornikoel J, Nieves-Morión M, Krauß N, Herrero A, et al. Intercellular diffusion of a fluorescent sucrose analog via the septal junctions in a filamentous cyanobacterium. MBio. 2015;6(2):e02109–14. doi: 10.1128/mBio.02109-14 25784700

72. Srirangan K, Pyne ME, Chou CP. Biochemical and genetic engineering strategies to enhance hydrogen production in photosynthetic algae and cyanobacteria. Bioresource technology. 2011;102(18):8589–604. doi: 10.1016/j.biortech.2011.03.087 21514821

73. Walsby AE. The permeability of heterocysts to the gases nitrogen and oxygen. Proc R Soc Lond B. 1985;226(1244):345–66.

74. Jensen BB, Cox RP. Effect of oxygen concentration on dark nitrogen fixation and respiration in cyanobacteria. Archives of Microbiology. 1983;135(4):287–92.

75. Tamagnini P, Axelsson R, Lindberg P, Oxelfelt F, Wünschiers R, Lindblad P. Hydrogenases and hydrogen metabolism of cyanobacteria. Microbiology and Molecular Biology Reviews. 2002;66(1):1–20. doi: 10.1128/MMBR.66.1.1-20.2002 11875125

76. Schilling N, Ehrnsperger K. Cellular differentiation of sucrose metabolism in Anabaena variabilis. Zeitschrift für Naturforschung C. 1985;40(11–12):776–9.

77. Winkenbach F, Wolk CP. Activities of enzymes of the oxidative and the reductive pentose phosphate pathways in heterocysts of a blue-green alga. Plant physiology. 1973;52(5):480–3. doi: 10.1104/pp.52.5.480 16658588

78. Summers ML, Wallis JG, Campbell EL, Meeks JC. Genetic evidence of a major role for glucose-6-phosphate dehydrogenase in nitrogen fixation and dark growth of the cyanobacterium Nostoc sp. strain ATCC 29133. Journal of bacteriology. 1995;177(21):6184–94. doi: 10.1128/jb.177.21.6184-6194.1995 7592384

79. Carrieri D, Wawrousek K, Eckert C, Yu J, Maness P-C. The role of the bidirectional hydrogenase in cyanobacteria. Bioresource technology. 2011;102(18):8368–77. doi: 10.1016/j.biortech.2011.03.103 21514820

80. Bothe H, Schmitz O, Yates MG, Newton WE. Nitrogen fixation and hydrogen metabolism in cyanobacteria. Microbiology and molecular biology reviews. 2010;74(4):529–51. doi: 10.1128/MMBR.00033-10 21119016

81. Sveshnikov D, Sveshnikova N, Rao K, Hall D. Hydrogen metabolism of mutant forms of Anabaena variabilis in continuous cultures and under nutritional stress. FEMS Microbiology Letters. 1997;147(2):297–301.

82. Masukawa H, Mochimaru M, Sakurai H. Disruption of the uptake hydrogenase gene, but not of the bidirectional hydrogenase gene, leads to enhanced photobiological hydrogen production by the nitrogen-fixing cyanobacterium Anabaena sp. PCC 7120. Applied Microbiology and Biotechnology. 2002;58(5):618–24. doi: 10.1007/s00253-002-0934-7 11956744

83. Oh Y-K, Raj SM, Jung GY, Park S. Current status of the metabolic engineering of microorganisms for biohydrogen production. Bioresource technology. 2011;102(18):8357–67. doi: 10.1016/j.biortech.2011.04.054 21733680

84. Hallenbeck PC, Benemann JR. Biological hydrogen production; fundamentals and limiting processes. International journal of hydrogen energy. 2002;27(11–12):1185–93.

85. Triana J, Montagud A, Siurana M, Urchueguía A, Gamermann D, Torres J, et al. Generation and evaluation of a genome-scale metabolic network model of Synechococcus elongatus PCC7942. Metabolites. 2014;4(3):680–98. doi: 10.3390/metabo4030680 25141288

86. Klanchui A, Khannapho C, Phodee A, Cheevadhanarak S, Meechai A. iAK692: A genome-scale metabolic model of Spirulina platensis C1. BMC systems biology. 2012;6(1):71.


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