Home LiteratureArticle Details
PMID: 18767191 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Genome-scale model for Clostridium acetobutylicum: Part II. Development of specific proton flux states and numerically determined sub-systems.

Biotechnology and bioengineering ·Vol. 101 ·No. 5 ·2008-12-01 ·Pages 1053-71

Senger RS, Papoutsakis ET

Abstract

A regulated genome-scale model for Clostridium acetobutylicum ATCC 824 was developed based on its metabolic network reconstruction. To aid model convergence and limit the number of flux-vector possible solutions (the size of the phenotypic solution space), modeling strategies were developed to impose a new type of constraint at the endo-exo-metabolome interface. This constraint is termed the specific proton flux state, and its use enabled accurate prediction of the extracellular medium pH during vegetative growth of batch cultures. The specific proton flux refers to the influx or efflux of free protons (per unit biomass) across the cell membrane. A specific proton flux state encompasses a defined range of specific proton fluxes and includes all metabolic flux distributions resulting in a specific proton flux within this range. Effective simulation of time-course batch fermentation required the use of independent flux balance solutions from an optimum set of specific proton flux states. Using a real-coded genetic algorithm to optimize temporal bounds of specific proton flux states, we show that six separate specific proton flux states are required to model vegetative-growth metabolism and accurately predict the extracellular medium pH. Further, we define the apparent proton flux stoichiometry per weak acids efflux and show that this value decreases from approximately 3.5 mol of protons secreted per mole of weak acids at the start of the culture to approximately 0 at the end of vegetative growth. Calculations revealed that when specific weak acids production is maximized in vegetative growth, the net proton exchange between the cell and environment occurs primarily through weak acids efflux (apparent proton flux stoichiometry is 1). However, proton efflux through cation channels during the early stages of acidogenesis was found to be significant. We have also developed the concept of numerically determined sub-systems of genome-scale metabolic networks here as a sub-network with a one-dimensional null space basis set. A numerically determined sub-system was constructed in the genome-scale metabolic network to study the flux magnitudes and directions of acetylornithine transaminase, alanine racemase, and D-alanine transaminase. These results were then used to establish additional constraints for the genome-scale model.

MeSH Terms
Acids/analysis,metabolism Alanine Racemase/metabolism Biomass Cell Growth Processes/genetics Clostridium acetobutylicum/growth & development,metabolism Computational Biology/methods D-Alanine Transaminase/metabolism Extracellular Fluid/chemistry Fermentation/physiology Hydrogen-Ion Concentration Ion Transport/physiology Kinetics Metabolic Networks and Pathways/genetics Metabolome/physiology Models, Biological Protons Signal Transduction Systems Integration Transaminases/metabolism
Chemicals
Acids Protons Transaminases acetylornithine transaminase D-Alanine Transaminase Alanine Racemase
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Senger Ryan S
Delaware Biotechnology Institute, University of Delaware, 15 Innovation Way, Newark, Delaware 19711, USA. [email protected]
Papoutsakis Eleftherios T
References (55)
55 references, click to expand
  1. Genome-scale models of microbial cells: evaluating the consequences of constraints.
    Nat Rev Microbiol. 2004 Nov;2(11):886-97 PMID: 15494745
  2. Development of a culture sub-population induction model: signaling pathways synergy and taxanes production by Taxus canadensis.
    Biotechnol Prog. 2006 Nov-Dec;22(6):1671-82 PMID: 17137317
  3. Estimation of O(2) and CO(2) Solubility in Microbial Culture Media.
    Biotechnol Prog. 1999 Oct 1;15(5):923-927 PMID: 10514263
  4. Gas chromatography and gateway sensors for on-line state estimation of complex fermentations (butanol-acetone fermentation).
    Biotechnol Bioeng. 1985 Aug;27(8):1246-57 PMID: 18553808
  5. Acetone-butanol fermentation revisited.
    Microbiol Rev. 1986 Dec;50(4):484-524 PMID: 3540574
  6. Genome-scale microbial in silico models: the constraints-based approach.
    Trends Biotechnol. 2003 Apr;21(4):162-9 PMID: 12679064
  7. Metabolic flux analysis elucidates the importance of the acid-formation pathways in regulating solvent production by Clostridium acetobutylicum.
    Metab Eng. 1999 Jul;1(3):206-13 PMID: 10937935
  8. The transporter classification (TC) system, 2002.
    Crit Rev Biochem Mol Biol. 2002;37(5):287-337 PMID: 12449427
  9. The next wave in metabolome analysis.
    Trends Biotechnol. 2005 Nov;23(11):544-6 PMID: 16154652
  10. Incorporating metabolic flux ratios into constraint-based flux analysis by using artificial metabolites and converging ratio determinants.
    J Biotechnol. 2007 May 10;129(4):696-705 PMID: 17408794
  11. Regulation of carbon and electron flow in Clostridium acetobutylicum grown in chemostat culture at neutral pH on mixtures of glucose and glycerol.
    J Bacteriol. 1994 Mar;176(5):1443-50 PMID: 8113186
  12. Matrix formalism to describe functional states of transcriptional regulatory systems.
    PLoS Comput Biol. 2006 Aug 11;2(8):e101 PMID: 16895435
  13. Solventogenesis in Clostridium acetobutylicum fermentations related to carboxylic acid and proton concentrations.
    Biotechnol Bioeng. 1988 Sep 20;32(7):843-52 PMID: 18587795
  14. Transcriptional analysis of spo0A overexpression in Clostridium acetobutylicum and its effect on the cell's response to butanol stress.
    J Bacteriol. 2004 Apr;186(7):1959-71 PMID: 15028679
  15. Properties and function of clostridial membrane ATPase.
    Biochim Biophys Acta. 1976 Jun 8;430(3):434-44 PMID: 132964
  16. Using large-scale perturbations in gene network reconstruction.
    BMC Bioinformatics. 2005 Jan 19;6:11 PMID: 15659246
  17. Genome-scale model for Clostridium acetobutylicum: Part I. Metabolic network resolution and analysis.
    Biotechnol Bioeng. 2008 Dec 1;101(5):1036-52 PMID: 18767192
  18. Equilibrium compositions of solutions of biochemical species and heats of biochemical reactions.
    Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3268-71 PMID: 11607175
  19. Acetone and Butanol Production by Clostridium acetobutylicum in a Synthetic Medium.
    Appl Environ Microbiol. 1982 Dec;44(6):1318-24 PMID: 16346149
  20. Changes in wall teichoic acid during the rod-sphere transition of Bacillus subtilis 168.
    J Bacteriol. 1994 Dec;176(23):7252-9 PMID: 7961496
  21. ABC-ATPases, adaptable energy generators fuelling transmembrane movement of a variety of molecules in organisms from bacteria to humans.
    J Mol Biol. 1999 Oct 22;293(2):381-99 PMID: 10529352
  22. Putative regulatory sites unraveled by network-embedded thermodynamic analysis of metabolome data.
    Mol Syst Biol. 2006;2:2006.0034 PMID: 16788595
  23. Dynamics of genomic-library enrichment and identification of solvent tolerance genes for Clostridium acetobutylicum.
    Appl Environ Microbiol. 2007 May;73(9):3061-8 PMID: 17337545
  24. Carbohydrate transport in bacteria.
    Microbiol Rev. 1980 Sep;44(3):385-418 PMID: 6999324
  25. Systems approach to refining genome annotation.
    Proc Natl Acad Sci U S A. 2006 Nov 14;103(46):17480-4 PMID: 17088549
  26. Stoichiometric modeling of Clostridium acetobutylicum fermentations with non-linear constraints.
    J Biotechnol. 1999 May 28;71(1-3):191-205 PMID: 10483106
  27. A comparative genomic view of clostridial sporulation and physiology.
    Nat Rev Microbiol. 2005 Dec;3(12):969-78 PMID: 16261177
  28. TCDB: the Transporter Classification Database for membrane transport protein analyses and information.
    Nucleic Acids Res. 2006 Jan 1;34(Database issue):D181-6 PMID: 16381841
  29. Fermentation equations for propionic-acid bacteria and production of assorted oxychemicals from various sugars.
    Biotechnol Bioeng. 1985 Jan;27(1):67-80 PMID: 18553577
  30. In silico genome-scale reconstruction and validation of the Staphylococcus aureus metabolic network.
    Biotechnol Bioeng. 2005 Dec 30;92(7):850-64 PMID: 16155945
  31. DNA array-based transcriptional analysis of asporogenous, nonsolventogenic Clostridium acetobutylicum strains SKO1 and M5.
    J Bacteriol. 2003 Aug;185(15):4539-47 PMID: 12867463
  32. Equations and calculations for fermentations of butyric acid bacteria.
    Biotechnol Bioeng. 1984 Feb;26(2):174-87 PMID: 18551704
  33. A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in gram-positive bacteria.
    Microbiol Mol Biol Rev. 2003 Dec;67(4):686-723 PMID: 14665680
  34. Levels of thermodynamic treatment of biochemical reaction systems.
    Biophys J. 1993 Sep;65(3):1243-54 PMID: 8241405
  35. The effect of pH on nitrogen supply, cell lysis, and solvent production in fermentations of Clostridium acetobutylicum.
    Biotechnol Bioeng. 1985 May;27(5):681-94 PMID: 18553724
  36. Northern, morphological, and fermentation analysis of spo0A inactivation and overexpression in Clostridium acetobutylicum ATCC 824.
    J Bacteriol. 2002 Jul;184(13):3586-97 PMID: 12057953
  37. Genome-scale thermodynamic analysis of Escherichia coli metabolism.
    Biophys J. 2006 Feb 15;90(4):1453-61 PMID: 16299075
  38. Transcriptional analysis of product-concentration driven changes in cellular programs of recombinant Clostridium acetobutylicumstrains.
    Biotechnol Bioeng. 2003 Dec 30;84(7):842-54 PMID: 14708125
  39. Reconstruction and validation of Saccharomyces cerevisiae iND750, a fully compartmentalized genome-scale metabolic model.
    Genome Res. 2004 Jul;14(7):1298-309 PMID: 15197165
  40. Semi-mechanistic partial buffer approach to modeling pH, the buffer properties, and the distribution of ionic species in complex solutions.
    J Agric Food Chem. 2006 Aug 9;54(16):6021-9 PMID: 16881711
  41. k-Cone analysis: determining all candidate values for kinetic parameters on a network scale.
    Biophys J. 2005 Mar;88(3):1616-25 PMID: 15626710
  42. Transcriptional program of early sporulation and stationary-phase events in Clostridium acetobutylicum.
    J Bacteriol. 2005 Oct;187(20):7103-18 PMID: 16199581
  43. A genome-scale computational study of the interplay between transcriptional regulation and metabolism.
    Mol Syst Biol. 2007;3:101 PMID: 17437026
  44. Equations and calculations of product yields and preferred pathways for butanediol and mixed-acid fermentations.
    Biotechnol Bioeng. 1985 Jan;27(1):50-66 PMID: 18553576
  45. Timing and genetic regulation of commitment to sporulation in Bacillus subtilis.
    Microbiology (Reading). 1996 Dec;142 (Pt 12):3445-52 PMID: 9244562
  46. Thermodynamics-based metabolic flux analysis.
    Biophys J. 2007 Mar 1;92(5):1792-805 PMID: 17172310
  47. Purification and reconstitution into proteoliposomes of the F1F0 ATP synthase from the obligately anaerobic gram-positive bacterium Clostridium thermoautotrophicum.
    J Bacteriol. 1997 Mar;179(5):1714-20 PMID: 9045833
  48. An expanded genome-scale model of Escherichia coli K-12 (iJR904 GSM/GPR).
    Genome Biol. 2003;4(9):R54 PMID: 12952533
  49. Monte Carlo sampling can be used to determine the size and shape of the steady-state flux space.
    J Theor Biol. 2004 Jun 21;228(4):437-47 PMID: 15178193
  50. Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum.
    J Bacteriol. 2001 Aug;183(16):4823-38 PMID: 11466286
  51. Identifying constraints that govern cell behavior: a key to converting conceptual to computational models in biology?
    Biotechnol Bioeng. 2003 Dec 30;84(7):763-72 PMID: 14708117
  52. Reverse engineering gene networks: integrating genetic perturbations with dynamical modeling.
    Proc Natl Acad Sci U S A. 2003 May 13;100(10):5944-9 PMID: 12730377
  53. Transcriptional analysis of butanol stress and tolerance in Clostridium acetobutylicum.
    J Bacteriol. 2004 Apr;186(7):2006-18 PMID: 15028684
  54. Developmental commitment in a bacterium.
    Cell. 2005 May 6;121(3):401-9 PMID: 15882622
  55. Molecular genetics and the initiation of solventogenesis in Clostridium beijerinckii (formerly Clostridium acetobutylicum) NCIMB 8052.
    FEMS Microbiol Rev. 1995 Oct;17(3):275-85 PMID: 7576769
Article Info
Journal
Biotechnology and bioengineering
Abbr.
Biotechnol Bioeng
ISSN
1097-0290
Published
2008-12-01
Pages
1053-71
Language
English
Region
United States
NLM ID
7502021
PMCID
PMC2745297
Subset
IM
Grants
NIGMS NIH HHS · F32 GM078947-02 · United States
NIGMS NIH HHS · F32 GM078947-03 · United States
NIGMS NIH HHS · F32 GM078947-01A1 · United States
NIGMS NIH HHS · F32GM078947 · United States
NIGMS NIH HHS · F32 GM078947 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]