Genome scale metabolic modeling of the riboflavin overproducer Ashbya gossypii

Biotechnology and Bioengineering

Volumn 111, Issue 6, 2014, Pages 1191-1199

  Ledesma Amaro, Rodrigo ^a   Kerkhoven, Eduard J ^b   Revuelta, José Luis ^a   Nielsen, Jens ^b  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

Author keywords

Ashbya gossypii; Eremothecium; Genome scale metabolic model; Microbial biotechnology; Riboflavin; Systems metabolic engineering

Indexed keywords

BIOTECHNOLOGY; METABOLIC ENGINEERING; METABOLISM; SUBSTRATES; YEAST;

ASHBYA GOSSYPII; EREMOTHECIUM; GENOME-SCALE METABOLIC MODELING; MICROBIAL BIOTECHNOLOGY; RIBOFLAVIN; SYSTEMS METABOLIC ENGINEERINGS;

GENES;

RIBOFLAVIN;

AMINO ACID METABOLISM; ARTICLE; ASHBYA GOSSYPII; BIOSYNTHESIS; CARBON SOURCE; CITRIC ACID CYCLE; COMPUTER MODEL; CONSENSUS SEQUENCE; CYTOPLASM; DOWN REGULATION; EREMOTHECIUM; FATTY ACID OXIDATION; FUNGAL GENETICS; FUNGUS GROWTH; GENETIC ENGINEERING; GENETIC MODEL; GENOME SCALE METABOLIC MODELING; GLUCONEOGENESIS; GLYCOLYSIS; GROWTH CURVE; LIPID METABOLISM; METABOLIC ENGINEERING; MITOCHONDRION; NITROGEN UTILIZATION; NONHUMAN; NUCLEOTIDE METABOLISM; NUTRIENT SUPPLY; OXIDATIVE PHOSPHORYLATION; PENTOSE PHOSPHATE CYCLE; PEROXISOME; PROTEIN DEGRADATION; PROTEIN METABOLISM; PURINE METABOLISM; PURINE SYNTHESIS; TRANSCRIPTOMICS; UPREGULATION; BIOLOGICAL MODEL; COMPUTER SIMULATION; FUNGAL GENOME; GENE REGULATORY NETWORK; GENETICS; METABOLISM; SYSTEMS BIOLOGY;

EREMOTHECIUM; EREMOTHECIUM GOSSYPII; EUKARYOTA; FUNGI; SACCHAROMYCES CEREVISIAE;

BIOSYNTHETIC PATHWAYS; COMPUTER SIMULATION; EREMOTHECIUM; GENE REGULATORY NETWORKS; GENOME, FUNGAL; MODELS, BIOLOGICAL; RIBOFLAVIN; SYSTEMS BIOLOGY;

EID: 84899627204     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.25167     Document Type: Article

References (57)

1. Agren R, Liu L, Shoaie S, Vongsangnak W, Nookaew I, Nielsen J. 2013a. The RAVEN toolbox and its use for generating a genome-scale metabolic model for Penicillium chrysogenum. PLoS Comput Biol 9(3):e1002980.
2. Agren R, Otero JM, Nielsen J. 2013b. Genome-scale modeling enables metabolic engineering of Saccharomyces cerevisiae for succinic acid production. J Ind Microbiol Biotechnol 40(7):735-747.
3. Bordel S, Agren R, Nielsen J. 2010. Sampling the solution space in genome-scale metabolic networks reveals transcriptional regulation in key enzymes. PLoS Comput Biol 6(7):e1000859.
4. Brachat S, Dietrich FS, Voegeli S, Zhang Z, Stuart L, Lerch A, Gates K, Gaffney T, Philippsen P. 2003. Reinvestigation of the Saccharomyces cerevisiae genome annotation by comparison to the genome of a related fungus: Ashbya gossypii. Genome Biol 4(7):R45.
5. Caspeta L, Nielsen J. 2013. Toward systems metabolic engineering of Aspergillus and Pichia species for the production of chemicals and biofuels. Biotechnol J 8(5):534-544.
6. Caspi R, Altman T, Dreher K, Fulcher CA, Subhraveti P, Keseler IM, Kothari A, Krummenacker M, Latendresse M, Mueller LA, Paley S, Popescu L, Pujar A, Shearer AG, Zhang P, Karp PD. 2012. The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res 40(Database issue):D742-D753.
7. Cherry JM, Hong EL, Amundsen C, Balakrishnan R, Binkley G, Chan ET, Christie KR, Costanzo MC, Dwight SS, Engel SR, et al. 2012. Saccharomyces genome database: The genomics resource of budding yeast. Nucleic Acids Res 40(Database issue):D700-D705.
8. Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, Sevier CS, Ding H, Koh JL, Toufighi K, Mostafavi S, et al. 2010. The genetic landscape of a cell. Science 327(5964):425-431.
9. Cvijovic M, Olivares-Hernandez R, Agren R, Dahr N, Vongsangnak W, Nookaew I, Patil KR, Nielsen J. 2010. BioMet Toolbox: Genome-wide analysis of metabolism. Nucleic Acids Res 38(Web Server issue):W144-W149.
10. Demain AL. 1972. Riboflavin oversynthesis. Annu Rev Microbiol 26:369-388.
11. Dietrich FS, Voegeli S, Brachat S, Lerch A, Gates K, Steiner S, Mohr C, Pohlmann R, Luedi P, Choi S, et al. 2004. The Ashbya gossypii genome as a tool for mapping the ancient Saccharomyces cerevisiae genome. Science 304(5668):304-307.
12. Farries EHM, Bell AF. 1930. On the metabolism of Nematospora gossypii and related fungi, with special reference to the source of nitrogen. Ann Bot 44:423-455.
13. Finlayson MR, Helfer-Hungerbuhler AK, Philippsen P. 2011. Regulation of exit from mitosis in multinucleate Ashbya gossypii cells relies on a minimal network of genes. Mol Biol Cell 22(17):3081-3093.
14. Garcia-Albornoz MA, Nielsen J. 2013. Application of genome-scale metabolic models in metabolic engineering Indus Biotechnol 9(4):203-214.
15. Gattiker A, Rischatsch R, Demougin P, Voegeli S, Dietrich FS, Philippsen P, Primig M. 2007. Ashbya Genome Database 3.0: A cross-species genome and transcriptome browser for yeast biologists. BMC Genom 8:9.
16. Hermida L, Brachat S, Voegeli S, Philippsen P, Primig M. 2005. The Ashbya Genome Database (AGD)-A tool for the yeast community and genome biologists. Nucleic Acids Res 33(Database issue):D348-D352.
17. Ibarra RU, Edwards JS, Palsson BO. 2002. Escherichia coli K-12 undergoes adaptive evolution to achieve in silico predicted optimal growth. Nature 420(6912):186-189.
18. Jimenez A, Santos MA, Pompejus M, Revuelta JL. 2005. Metabolic engineering of the purine pathway for riboflavin production in Ashbya gossypii. Appl Environ Microbiol 71(10):5743-5751.
19. Jimenez A, Santos MA, Revuelta JL. 2008. Phosphoribosyl pyrophosphate synthetase activity affects growth and riboflavin production in Ashbya gossypii. BMC Biotechnol 8:67.
20. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M. 2012. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 40(Database issue):D109-D114.
21. Kato T, Park EY. 2012. Riboflavin production by Ashbya gossypii. Biotechnol Lett 34(4):611-618.
22. 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(4):617-623.
23. Kuepfer L, Sauer U, Blank LM. 2005. Metabolic functions of duplicate genes in Saccharomyces cerevisiae. Genome Res 15(10):1421-1430.
24. Kurtzman CP, Fell JW, Boekhout T. 2011. The yeast: A taxonomic study. 5th edn. Elsevier, Amsterdam Volume 2, Part IVb.
25. Ledesma-Amaro R, Jimenez A, Santos MA, Revuelta JL. 2013a. Biotechnological production of feed nucleotides by microbial strain improvement. Process Biochem 48(9):1263-1270.
26. Ledesma-Amaro R, Jimenez A, Santos MA, Revuelta JL. 2013b. Microbial production of vitamins. Book chapter in: Microbial production of food ingredients, enzymes and nutraceuticals, Sawston, Cambridge, UK: Woodhead Publishing Series in Food Science. Technology and Nutrition No. 246.
27. Ledesma-Amaro R, Santos MA, Jiménez A, Revuelta JL. 2013c. Strain design of Ashbya gossypii for single-cell oil production. Applied and Environmental Microbiology, doi: 10.1128/aem.03560-13. AEM.03560-13 published ahead of print 6 December 2013.
28. Lim SH, Ming H, Park EY, Choi JS. 2003. Improvement of riboflavin production using mineral support in the culture of Ashbya gossypii. Food Technol Biotechnol 41(2):137-144.
29. Mateos L, Jimenez A, Revuelta JL, Santos MA. 2006. Purine biosynthesis, riboflavin production, and trophic-phase span are controlled by a Myb-related transcription factor in the fungus Ashbya gossypii. Appl Environ Microbiol 72(7):5052-5060.
30. Mickelson MN. 1950. The metabolism of glucose by Ashbya gossypii. J Bacteriol 59(5):659-666.
31. Monschau N, Sahm H, Stahmann K. 1998. Threonine aldolase overexpression plus threonine supplementation enhanced riboflavin production in Ashbya gossypii. Appl Environ Microbiol 64(11):4283-4290.
32. Osterlund T, Nookaew I, Bordel S, Nielsen J. 2013. Mapping condition-dependent regulation of metabolism in yeast through genome-scale modeling. BMC Syst Biol 7:36.
33. Otero JM, Cimini D, Patil KR, Poulsen SG, Olsson L, Nielsen J. 2013. Industrial systems biology of Saccharomyces cerevisiae enables novel succinic acid cell factory. PLoS ONE 8(1):e54144.
34. Park EY, Ito Y, Nariyama M, Sugimoto T, Lies D, Kato T. 2011. The improvement of riboflavin production in Ashbya gossypii via disparity mutagenesis and DNA microarray analysis. Appl Microbiol Biotechnol 91(5):1315-1326.
35. Park EY, Zhang JH, Tajima S, Dwiarti L. 2007a. Isolation of Ashbya gossypii mutant for an improved riboflavin production targeting for biorefinery technology. J Appl Microbiol 103(2):468-476.
36. Park JH, Lee KH, Kim TY, Lee SY. 2007b. Metabolic engineering of Escherichia coli for the production of L-valine based on transcriptome analysis and in silico gene knockout simulation. Proc Natl Acad Sci U S A 104(19):7797-7802.
37. Park JM, Kim TY, Lee SY. 2009. Constraints-based genome-scale metabolic simulation for systems metabolic engineering. Biotechnol Adv 27(6):979-988.
38. Patil KR, Nielsen J. 2005. Uncovering transcriptional regulation of metabolism by using metabolic network topology. Proc Natl Acad Sci U S A 102(8):2685-2689.
39. Ribeiro O, Domingues L, Penttila M, Wiebe MG. 2012. Nutritional requirements and strain heterogeneity in Ashbya gossypii. J Basic Microbiol 52(5):582-589.
40. Ribeiro O, Magalhaes F, Aguiar TQ, Wiebe MG, Penttila M, Domingues L. 2013. Random and direct mutagenesis to enhance protein secretion in Ashbya gossypii. Bioengineered 4(5):322-331.
41. Ribeiro O, Wiebe M, Ilmen M, Domingues L, Penttila M. 2010. Expression of Trichoderma reesei cellulases CBHI and EGI in Ashbya gossypii. Appl Microbiol Biotechnol 87(4):1437-1446.
42. Rischatsch R. 2007. Transcriptinoal profiling of the model organism A. gossypii: Comparison of life cycle stages and transcription factor deletions. PhD thesis.
43. Scalcinati G, Otero JM, Van Vleet JR, Jeffries TW, Olsson L, Nielsen J. 2012. Evolutionary engineering of Saccharomyces cerevisiae for efficient aerobic xylose consumption. FEMS Yeast Res 12(5):582-597.
44. Schlupen C, Santos MA, Weber U, de Graaf A, Revuelta JL, Stahmann KP. 2003. Disruption of the SHM2 gene, encoding one of two serine hydroxymethyltransferase isoenzymes, reduces the flux from glycine to serine in Ashbya gossypii. Biochem J 369(Pt 2):263-273.
45. Schmitz HP, Philippsen P. 2011. Evolution of multinucleated Ashbya gossypii hyphae from a budding yeast-like ancestor. Fungal Biol 115(6):557-568.
46. Shi S, Chen T, Zhang Z, Chen X, Zhao X. 2009. Transcriptome analysis guided metabolic engineering of Bacillus subtilis for riboflavin production. Metab Eng 11(4-5):243-252.
47. Stahmann KP, Arst HN, Jr., Althofer H, Revuelta JL, Monschau N, Schlupen C, Gatgens C, Wiesenburg A, Schlosser T. 2001. Riboflavin, overproduced during sporulation of Ashbya gossypii, protects its hyaline spores against ultraviolet light. Environ Microbiol 3(9):545-550.
48. Stahmann KP, Kupp C, Feldmann SD, Sahm H. 1994. Formation and degradation of lipid bodies found in the riboflavin-producing fungus Ashbya gossypii. Appl Microbiol Biotechnol 42(1):121-127.
49. Stahmann KP, Revuelta JL, Seulberger H. 2000. Three biotechnical processes using Ashbya gossypii, Candida famata, or Bacillus subtilis compete with chemical riboflavin production. Appl Microbiol Biotechnol 53(5):509-516.
50. Sugimoto T, Kanamasa S, Kato T, Park EY. 2009. Importance of malate synthase in the glyoxylate cycle of Ashbya gossypii for the efficient production of riboflavin. Appl Microbiol Biotechnol 83(3):529-539.
51. van Zyl C, Prior BA, Kilian SG, Kock JL. 1989. D-xylose utilization by Saccharomyces cerevisiae. J Gen Microbiol 135(11):2791-2798.
52. Varemo L, Nielsen J, Nookaew I. 2013. Enriching the gene set analysis of genome-wide data by incorporating directionality of gene expression and combining statistical hypotheses and methods. Nucleic Acids Res 41(8):4378-4391.
53. Vongsangnak W, Olsen P, Hansen K, Krogsgaard S, Nielsen J. 2008. Improved annotation through genome-scale metabolic modeling of Aspergillus oryzae. BMC Genom 9:245.
54. Wendland J, Ayad-Durieux Y, Knechtle P, Rebischung C, Philippsen P. 2000. PCR-based gene targeting in the filamentous fungus Ashbya gossypii. Gene 242(1-2):381-391.
55. Wendland J, Dunkler A, Walther A. 2011. Characterization of alpha-factor pheromone and pheromone receptor genes of Ashbya gossypii. FEMS Yeast Res 11(5):418-429.
56. Wendland J, Walther A. 2005. Ashbya gossypii: A model for fungal developmental biology. Nature reviews. Microbiology 3(5):421-429.
57. Wolfe KH, Shields DC. 1997. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387(6634):708-713.