Genome-scale metabolic model for the green alga chlorella vulgaris UTEX 395 accurately predicts phenotypes under autotrophic, heterotrophic, and mixotrophic growth conditions

Plant Physiology

Volumn 172, Issue 1, 2016, Pages 589-602

  Zuñiga, Cristal ^a   Li, Chien Ting ^b   Huelsman, Tyler ^a   Levering, Jennifer ^a   Zielinski, Daniel C ^a   McConnell, Brian O ^c   Long, Christopher P ^c   Knoshaug, Eric P ^d   Guarnieri, Michael T ^d   Antoniewicz, Maciek R ^c   Betenbaugh, Michael J ^b   Zengler, Karsten ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b Johns Hopkins University   (United States)

^c UNIVERSITY OF DELAWARE   (United States)

^d NATIONAL RENEWABLE ENERGY LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CARBON; PIGMENT;

AUTOTROPHY; BIOLOGICAL MODEL; BIOMASS; CHLORELLA VULGARIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; HETEROTROPHY; METABOLISM; MICROALGA; PLANT GENOME;

AMINO ACIDS; AUTOTROPHIC PROCESSES; BIOMASS; CARBON; CHLORELLA VULGARIS; GENOME, PLANT; HETEROTROPHIC PROCESSES; METABOLIC NETWORKS AND PATHWAYS; MICROALGAE; MODELS, BIOLOGICAL; PIGMENTS, BIOLOGICAL;

EID: 84984903685     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.16.00593     Document Type: Article

References (72)

1. Agren R, Liu L, Shoaie S, Vongsangnak W, Nookaew I, Nielsen J (2013) The RAVEN toolbox and its use for generating a genome-scale metabolic model for Penicillium chrysogenum. PLOS Comput Biol 9: e1002980
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410
3. Antoniewicz MR, Kelleher JK, Stephanopoulos G (2007) Accurate assessment of amino acid mass isotopomer distributions for metabolic flux analysis. Anal Chem 79: 7554-7559
4. Antoniewicz MR, Kelleher JK, Stephanopoulos G (2011) Measuring deuterium enrichment of glucose hydrogen atoms by gas chromatography/mass spectrometry. Anal Chem 83: 3211-3216
5. Baroukh C, Muñoz-Tamayo R, Steyer JP, Bernard O (2015) A state of the art of metabolic networks of unicellular microalgae and cyanobacteria for biofuel production. Metab Eng 30: 49-60
6. Bellou S, Baeshen MN, Elazzazy AM, Aggeli D, Sayegh F, Aggelis G (2014) Microalgal lipids biochemistry and biotechnological perspectives. Biotechnol Adv 32: 1476-1493
7. Boyle NR, Morgan JA (2009) Flux balance analysis of primary metabolism in Chlamydomonas reinhardtii. BMC Syst Biol 3: 4
8. Caspi R, Altman T, Billington R, Dreher K, Foerster H, Fulcher CA, Holland TA, Keseler IM, Kothari A, Kubo A, et al (2014) The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res 42: D459-D471
9. Chaiboonchoe A, Dohai BS, Cai H, Nelson DR, Jijakli K, Salehi-Ashtiani K (2014) Microalgal metabolic network model refinement through highthroughput functional metabolic profiling. Front Bioeng Biotechnol 2: 68
10. Chang RL, Ghamsari L, Manichaikul A, Hom EFY, Balaji S, Fu W, Shen Y, Hao T, Palsson BØ, Salehi-Ashtiani K, et al (2011) Metabolic network reconstruction of Chlamydomonas offers insight into light-driven algal metabolism. Mol Syst Biol 7: 518
11. Dansen TB, Pap EHW, Wanders RJ, Wirtz KW (2001) Targeted fluorescent probes in peroxisome function. Histochem J 33: 65-69
12. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, et al (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36: W465-W469
13. Doucha J, Lívanský K (2006) Productivity, CO2/O2 exchange and hydraulics in outdoor open high density microalgal (Chlorella sp.) photobioreactors operated in a middle and southern European climate. J Appl Phycol 18: 811-826
14. Ebrahim A, Lerman JA, Palsson BO, Hyduke DR (2013) COBRApy: constraints-based reconstruction and analysis for python. BMC Syst Biol 7: 74
15. Emanuelsson O, Nielsen H, von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8: 978-984
16. Espinosa-Gonzalez I, Parashar A, Bressler DC (2014) Heterotrophic growth and lipid accumulation of Chlorella protothecoides in whey permeate, a dairy by-product stream, for biofuel production. Bioresour Technol 155: 170-176
17. Faheed AF, Fattah ZA (2008) Effect of Chlorella vulgaris as bio-fertilizer on growth parameters and metabolic aspects of lettuce plant. J Agric Soc Sci 4: 165-169
18. Giordano M, Norici A, Forssen M, Eriksson M, Raven JA (2003) An anaplerotic role for mitochondrial carbonic anhydrase in Chlamydomonas reinhardtii. Plant Physiol 132: 2126-2134
19. Goss R, Garab G (2001) Non-photochemical chlorophyll fluorescence quenching and structural rearrangements induced by low pH in intact cells of Chlorella fusca (Chlorophyceae) and Mantoniella squamata (Prasinophyceae). Photosynth Res 67: 185-197
20. Gschloessl B, Guermeur Y, Cock JM (2008) HECTAR: a method to predict subcellular targeting in heterokonts. BMC Bioinformatics 9: 393
21. Guarnieri MT, Nag A, Smolinski SL, Darzins A, Seibert M, Pienkos PT (2011) Examination of triacylglycerol biosynthetic pathways via de novo transcriptomic and proteomic analyses in an unsequenced microalga. PLoS ONE 6: e25851
22. Guarnieri MT, Nag A, Yang S, Pienkos PT (2013) Proteomic analysis of Chlorella vulgaris: potential targets for enhanced lipid accumulation. J Proteomics 93: 245-253
23. Hanson J (1985) Membrane transport systems of plant mitochondria. Encycl Plant Physiol 18: 248-275
24. Hogetsu D, Miyachi S (1979) Role of carbonic anhydrase in photosynthetic CO2. Symp A Q J Mod Foreign Lit 20: 747-756
25. Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35: W585-W587
26. Johnson X, Alric J (2013) Central carbon metabolism and electron transport in Chlamydomonas reinhardtii: metabolic constraints for carbon partitioning between oil and starch. Eukaryot Cell 12: 776-793
27. Juneja A, Chaplen FWR, Murthy GS (2016) Genome scale metabolic reconstruction of Chlorella variabilis for exploring its metabolic potential for biofuels. Bioresour Technol 213: 103-110
28. Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M (2014) Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res 42: D199-D205
29. Killam A, Myers J (1956) A special effect of light on the growth of Chlorella vulgaris. Am J Bot 43: 569
30. Kim TY, Sohn SB, Kim YB, Kim WJ, Lee SY (2012) Recent advances in reconstruction and applications of genome-scale metabolic models. Curr Opin Biotechnol 23: 617-623
31. King ZA, Dräger A, Ebrahim A, Sonnenschein N, Lewis NE, Palsson BO (2015) Escher: a web application for building, sharing, and embedding data-rich visualizations of biological pathways. PLOS Comput Biol 11: e1004321
32. Komor E, Tanner W (1974) The hexose-proton cotransport system of chlorella: pH-dependent change in Km values and translocation constants of the uptake system. J Gen Physiol 64: 568-581
33. Levering J, Broddrick J, Zengler K (2015) Engineering of oleaginous organisms for lipid production. Curr Opin Biotechnol 36: 32-39
34. Liu CH, Chang CY, Liao Q, Zhu X, Chang JS (2013) Photoheterotrophic growth of Chlorella vulgaris ESP6 on organic acids from dark hydrogen fermentation effluents. Bioresour Technol 145: 331-336
35. Long CP, Antoniewicz MR (2014) Quantifying biomass composition by gas chromatography/mass spectrometry. Anal Chem 86: 9423-9427
36. Matthews BW (1975) Comparison of the predicted and observed secondary structure of T4 phage lysozyme. Biochim Biophys Acta 405: 442-451
37. McDonald AG, Boyce S, Moss GP, Dixon HBF, Tipton KF (2007) ExplorEnz: a MySQL database of the IUBMB enzyme nomenclature. BMC Biochem 8: 14
38. McWilliam H, Li W, Uludag M, Squizzato S, Park YM, Buso N, Cowley AP, Lopez R (2013) Analysis tool web services from the EMBL-EBI. Nucleic Acids Res 41: W597-W600
39. Miao X, Wu Q (2006) Biodiesel production from heterotrophic microalgal oil. Bioresour Technol 97: 841-846
40. Mitra D, van Leeuwen J, Lamsal B (2012) Heterotrophic/mixotrophic cultivation of oleaginous Chlorella vulgaris on industrial co-products. Algal Res 1: 40-48
41. Monk J, Nogales J, Palsson BO (2014) Optimizing genome-scale network reconstructions. Nat Biotechnol 32: 447-452
42. Muthuraj M, Palabhanvi B, Misra S, Kumar V, Sivalingavasu K, Das D (2013) Flux balance analysis of Chlorella sp. FC2 IITG under photoautotrophic and heterotrophic growth conditions. Photosynth Res 118: 167-179
43. Nakamura Y, Imamura M (1985) Regulation of ADP-glucose pyrophosphorylase from Chlorella vulgaris. Plant Physiol 78: 601-605
44. Nascimento IA, Cabanelas-Dominguez IT, Nunes JD, Nascimento MA, Sousa L, Sansone G (2015) Biodiesel yields and fuel quality as criteria for algal-feedstock selection: effects of CO2-supplementation and nutrient levels in cultures. Algal Res 8: 53-60
45. Nichols BW, James AT, Breuer J (1967) Interrelationships between fatty acid biosynthesis and acyl-lipid synthesis in Chlorella vulgaris. Biochem J 104: 486-496
46. 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: 2678-2683
47. Orth JD, Thiele I, Palsson BØ (2010) What is flux balance analysis? Nat Biotechnol 28: 245-248
48. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA, Gerdes S, Parrello B, Shukla M, et al (2014) The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res 42: D206-D214
49. Palsson BØ (2011) Systems Biology: Simulation of Dynamic Network States. Cambridge University Press, Cambridge, UK
50. Perez-Garcia O, Escalante FME, de-Bashan LE, Bashan Y (2011) Heterotrophic cultures of microalgae: metabolism and potential products. Water Res 45: 11-36
51. Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785-786
52. Ren Q, Paulsen IT (2007) Large-scale comparative genomic analyses of cytoplasmic membrane transport systems in prokaryotes. J Mol Microbiol Biotechnol 12: 165-179
53. Safi C, Zebib B, Merah O, Pontalier PY, Vaca-Garcia C (2014) Morphology, composition, production, processing and applications of Chlorella vulgaris: a review. Renew Sustain Energy Rev 35: 265-278
54. Saha R, Suthers PF, Maranas CD (2011) Zea mays iRS1563: a comprehensive genome-scale metabolic reconstruction of maize metabolism. PLoS ONE 6: e21784
55. Saier MH Jr, Reddy VS, Tamang DG, Västermark A (2014) The trans porter classification database. Nucleic Acids Res 42: D251-D258
56. Savage N (2011) Algae: the scum solution. Nature 474: S15-S16
57. Scheer M, Grote A, Chang A, Schomburg I, Munaretto C, Rother M, Söhngen C, Stelzer M, Thiele J, Schomburg D (2011) BRENDA, the enzyme information system in 2011. Nucleic Acids Res 39: D670-D676
58. Schellenberger J, Park JO, Conrad TM, Palsson BØ (2010) BiGG: a Biochemical Genetic and Genomic knowledgebase of large scale metabolic reconstructions. BMC Bioinformatics 11: 213
59. Schellenberger J, Que R, Fleming RMT, Thiele I, Orth JD, Feist AM, Zielinski DC, Bordbar A, Lewis NE, Rahmanian S, et al (2011) Quantitative prediction of cellular metabolism with constraint-based models: the COBRA toolbox v2.0. Nat Protoc 6: 1290-1307
60. Schilling CH, Thakar R, Travnik E, Van Dien S, Wiback S (2008) SimPheny TM: A Computational Infrastructure for Systems Biology Shi XM, Chen F (1999) Production and rapid extraction of lutein and the other lipid-soluble pigments from Chlorella protothecoides grown under heterotrophic and mixotrophic conditions. Food/Nahrung 43: 109-113
61. Shrift A (1960) A role for methionine in division of Chlorella vulgaris. Plant Physiol 35: 510-515
62. Tabatabaei M, Tohidfar M, Jouzani GS, Safarnejad M, Pazouki M (2011) Biodiesel production from genetically engineered microalgae: future of bioenergy in Iran. Renew Sustain Energy Rev 15: 1918-1927
63. Thiele I, Palsson BØ (2010) A protocol for generating a high-quality genome-scale metabolic reconstruction. Nat Protoc 5: 93-121
64. Thompson GA (1996) Lipids and membrane function in green algae. Biochim Biophys Acta 1302: 17-45
65. UniProt Consortium (2015) UniProt: a hub for protein information. Nucleic Acids Res 43: D204-D212
66. Van Baalan C, Pulich WM, Brandeis MG (1973) Heterotrophic growth of the microalgae. Crit Rev Microbiol 2: 229-254
67. Wang B, Li Y, Wu N, Lan CQ (2008) CO2 bio-mitigation using microalgae. Appl Microbiol Biotechnol 79: 707-718
68. Wang Z, Zuidhof MJ (2004) Estimation of growth parameters using a nonlinear mixed Gompertz model. Poult Sci 83: 847-852
69. Wu C, Xiong W, Dai J, Wu Q (2015) Genome-based metabolic mapping and 13C flux analysis reveal systematic properties of an oleaginous microalga Chlorella protothecoides. Plant Physiol 167: 586-599
70. Xiong W, Li X, Xiang J, Wu Q (2008) High-density fermentation of microalga Chlorella protothecoides in bioreactor for microbio-diesel production. Appl Microbiol Biotechnol 78: 29-36
71. Yang C, Hua Q, Shimizu K (2000) Energetics and carbon metabolism during growth of microalgal cells under photoautotrophic, mixotrophic and cyclic light-autotrophic/dark-heterotrophic conditions. Biochem Eng J 6: 87-102
72. Zhu S, Wang Y, Huang W, Xu J, Wang Z, Xu J, Yuan Z (2014) Enhanced accumulation of carbohydrate and starch in Chlorella zofingiensis induced by nitrogen starvation. Appl Biochem Biotechnol 174: 2435-2445