[en] tDynamic stimulus-responses of Escherichia coli
DPD2085, yciG::LuxCDABE reporter strain, to glucose
pulses of different intensities (0.08, 0.4 and 1 gL
−1) were compared using glucose-limited chemostat cultures at dilution rate close to 0.15 h
−1. After at least five residence times,
the steady-state cultures were disturbed by a pulse of glucose, engendering conditions of glucose excess with concomitant oxygen limitation. In all conditions, glucose
consumption, acetate and formate accumulations followed
a linear relationship with time. The resulting specific uptake
and production rates as well as respiratory rates were rapidly
increased within the first seconds, which revealed a high
ability of E. coli strain to modulate its metabolism to a new
environment. For transition from glucose-excess to glucoselimited conditions, the cells rapidly re-established its
pseudo-steady state. The dynamics of transient responses
at the macroscopic viewpoint were shown to be independent
on the glucose pulse intensity in the tested range. On the
contrary, the E. coli biosensor yciG::luxCDABE revealed a
transcriptional induction of yciG gene promoter depending
on the quantities of the glucose added, through in situ and
online monitoring of the bioluminescence emitted by the
cells. Despite many studies describing the dynamics of the
transient response of E. coli to glucose perturbations, it is
the first time that a direct comparison is reported, using the
same experimental design (strain, medium and experimental
set up), to study the impact of the glucose pulse intensity on
the dynamics of microbial behaviour regarding growth,
respiration and metabolite productions.
Disciplines :
Biotechnology
Author, co-author :
Sunya, Sirichai
Delvigne, Frank ; Université de Liège - ULiège > Chimie et bio-industries > Bio-industries
Uribellarea, Jean-Louis
Molina-Jouve, Carole
Gorret, Nathalie
Language :
English
Title :
Comparison of the transient responses of Escherichia coli to a glucose pulse of various intensities
Alexeeva S, Hellingwerf KJ, de Mattos MJT (2003) Requirement of ArcA for redox regulation in Escherichia coli under microaerobic but not anaerobic or aerobic conditions. J Bacteriol 185:204-209
Bloemen HHJ, Wu L, van Gulik WM, Heijnen JJ, Verhaegen MHG (2003) Reconstruction of the O2 uptake rate and CO2 evolution rate on a time scale of seconds. AICHE J 49:1895-1908
Buchholz A, Hurlebaus J, Wandrey C, Takors R (2002) Metabolomics: Quantification of intracellular metabolite dynamics. Biomol Eng 19:5-15
Buziol S, Bashir I, Baumeister A, Claassen W, Noisommit-Rizzi N, Mailinger W, Reuss M (2002) New bioreactor-coupled rapid stopped-flow sampling technique for measurements of metabolite dynamics on a subsecond time scale. Biotechnol Bioeng 80:632-636
Bylund F, Collet E, Enfors SO, Larsson G (1998) Substrate gradient formation in the large-scale bioreactor lowers cell yield and increases by-product formation. Bioprocess Eng 18:171-180
Chassagnole C, Noisommit-Rizzi N, Schmid JW, Mauch K, Reuss M (2002) Dynamic modeling of the central carbon metabolism of Escherichia coli. Biotechnol Bioeng 79:53-73
Christensen LH, Schulze U, Nielsen J, Villadsen J (1995) Acoustic offgas analyzer for bioreactors-precision, accuracy and dynamics of detection. Chem Eng Sci 50:2601-2610
Clark DP (1989) The fermentation pathways of Escherichia coli. FEMS Microbiol Rev 63:223-234
de Jong H, Ranquet C, Ropers D, Pinel C, Geiselmann J (2010) Experimental and computational validation of models of fluorescent and luminescent reporter genes in bacteria. BMC Syst Biol 4:55-71
De Mey M, Taymaz-Nikerel H, Baart G, Waegeman H, Maertens J, Heijnen JJ, van Gulik WM (2010) Catching prompt metabolite dynamics in Escherichia coli with the BioScope at oxygen rich conditions. Metab Eng 12:477-487
Eiteman MA, Altman E (2006) Overcoming acetate in Escherichia coli recombinant protein fermentations. Trends In Biotechnology 24:530-536
Enfors SO, Jahic M, Rozkov A, Xu B, Hecker M, Jürgen B, Krüger E, Schweder T, Hamer G, O'Beirne D, Noisommit-Rizzi N, Reuss M, Boone L, Hewitt C, McFarlane C, Nienow A, Kovacs T, Trägardh C, Fuchs L, Revstedt J, Friberg PC, Hjertager BGBHS, Hjort S, Hoeks F, Lin H-Y, Neubauer P, van der Lans R, Luyben K, Vrabel P, Manelius A (2001) Physiological responses to mixing in large scale bioreactors. J Biotechnol 85:175-185
Gutknecht J, Bisson MA, Tosteson FC (1977) Diffusion of carbon dioxide through lipid bilayer membranes-effects of carbonicanhydrase, bicarbonate, and unstirred layers. J Gen Physiol 69:779-794
Harvey RJ (1970) Metabolic regulation in glucose-limited chemostat cultures of Escherichia coli. J Bacteriol 104:698-706
Hewitt CJ, Nebe-Von Caron G, Axelsson B, McFarlane CM, Nienow AW (2000) Studies related to the scale-up of high-cell-density Ecoli fed-batch fermentations using multiparameter flow cytometry: Effect of a changing microenvironment with respect to glucose and dissolved oxygen concentration. Biotechnol Bioeng 70:381-390
Hewitt CJ, Onyeaka H, Lewis G, Taylor IW, Nienow AW (2007) A comparison of high cell density fed-batch fermentations involving both induced and non-induced recombinant Escherichia coli under well-mixed small-scale and simulated poorly mixed largescale conditions. Biotechnol Bioeng 96:495-505
Hoque MA, Ushiyama H, Tomita M, Shimizu K (2005) Dynamic responses of the intracellular metabolite concentrations of the wild type and pykA mutant Escherichia coli against pulse addition of glucose or NH3 under those limiting continuous cultures. Biochem Eng J 26:38-49
Hoque MA, Attia K, Alattas O, Merican AF (2011) Metabolic flux distribution and mathematical models for dynamic simulation of carbon metabolism in Escherichia coli. Afr J Biotechnol 10:2340-2352
Ishii N, Nakahigashi K, Baba T, Robert M, Soga T, Kanai A, Hirasawa T, Naba M, Hirai K, Hoque A, Ho PY, Kakazu Y, Sugawara K, Igarashi S, Harada S, Masuda T, Sugiyama N, Togashi T, Hasegawa M, Takai Y, Yugi K, Arakawa K, Iwata N, Toya Y, Nakayama Y, Nishioka T, Shimizu K, Mori H, Tomita M (2007) Multiple high-Throughput analyses monitor the response of E. coli to perturbations. Science 316:593-597
Kalyanaraman G (2003) Construction and characterization of yciGFE mutants in Escherichia coli. Dissertation, Texas A&M University
Lara AR, Galindo E, Ramirez OT, Palomares LA (2006a) Living with heterogeneities in bioreactors. Mol Biotechnol 34:355-381
Lara AR, Leal L, Flores N, Gosset G, Bolivar F, Ramirez OT (2006b) Transcriptional and metabolic response of recombinant Escherichia coli to spatial dissolved oxygen tension gradients simulated in a scale-down system. Biotechnol Bioeng 93:372-385
Lara AR, Caspeta L, Gosset G, Bolivar F, Ramirez OT (2008) Utility of an Escherichia coli strain engineered in the substrate uptake system for improved culture performance at high glucose and cell concentrations: An alternative to fed-batch cultures. Biotechnol Bioeng 99:893-901
Lara AR, Taymaz-Nikerel H, Mashego MR, van Gulik WM, Heijnen JJ, Ramirez OT, van Winden WA (2009) Fast dynamic response of the fermentative metabolism of Escherichia coli to aerobic and anaerobic glucose pulses. Biotechnol Bioeng 104:1153-1161
Lin HY, Neubauer P (2000) Influence of controlled glucose oscillations on a fed-batch process of recombinant Escherichia coli. J Biotechnol 79:27-37
Lin HY, Mathiszik B, Xu B, Enfors SO, Neubauer P (2001) Determination of the maximum specific uptake capacities for glucose and oxygen in glucose-limited fed-batch cultivations of Escherichia coli. Biotechnol Bioeng 73:347-357
Link H, Anselment B, Weuster-Botz D (2010) Rapid media transition: An experimental approach for steady state analysis of metabolic pathways. Biotechnol Prog 26:1-10
Neubauer P, Junne S (2010) Scale-down simulators for metabolic analysis of large-scale bioprocesses. Curr Opin Biotechnol 21:114-121
Neubauer P, Haggstrom L, Enfors SO (1995) Influence of substrate oscillations on acetate formation and growth-yield in Escherichia coli glucose-limited fed-batch cultivations. Biotechnol Bioeng 47:139-146
Nienow AW (2009) Scale-up considerations based on studies at the bench scale in stirred bioreactors. J Chem Eng Jpn 42:789-796
O'Beirne D, Hamer G (2000) Oxygen availability and the growth of Escherichia coli W3110: A problem exacerbated by scale-up. Bioprocess Eng 23:487-494
Pecher A, Blaschkowski HP, Knappe K, Bock A (1982) Expression of pyruvate formate-lyase of Escherichia coli from the cloned structural gene. Arch Microbiol 132:365-371
Phue JN, Shiloach J (2005) Impact of dissolved oxygen concentration on acetate accumulation and physiology of E coli BL21, evaluating transcription levels of key genes at different dissolved oxygen conditions. Metab Eng 7:353-363
Roustan M, Pharamond JC, Line A (1999) Agitation Mélange Concepts théoriques de base. Technique-Ingénieur
Sawers G (1994) The hydrogenases and formate dehydrogenases of Escherichia coli. Antonie Van Leeuwenhoek 66:57-88
Schaefer U, Boos W, Takors R, Weuster-Botz D (1999) Automated sampling device for monitoring intracellular metabolite dynamics. Anal Biochem 270:88-96
Schaub J, Reuss M (2008) In vivo dynamics of glycolysis in Escherichia coli shows need for growth-rate dependent metabolome analysis. Biotechnol Prog 24:1402-1407
Slonczewski JL, Foster JW (1987) pH-regulated genes and survival at extreme pH. In: Neidhardt FC (ed) Escherichia coli and Salmonella typhimurium: Cellular and molecular biology. American Society for Microbiology, Washington, DC, pp 1539- 1549
Soini J, Ukkonen K, Neubauer P (2008) High cell density media for Escherichia coli are generally designed for aerobic cultivations- consequences for large-scale bioprocesses and shake flask cultures. Microb Cell Fact 7:26
Sunya S, Gorret N, Delvigne F, Uribelarrea JL, Molina-Jouve C (2012) Real-Time monitoring of metabolic shift and transcriptional induction of yciG:luxCDABE E. coli reporter strain to a glucose pulse of different concentrations. J Biotechnol 157:379-390
Taymaz-Nikerel H, van Gulik WM, Heijnen JJ (2011) Escherichia coli responds with a rapid and large change in growth rate upon a shift from glucose-limited to glucose-excess conditions. Metab Eng 13:307-318
Theobald U, MailingerW, Reuss M, Rizzi M(1993) In vivo analysis of glucose-induced fast changes in yeast adenine-nucleotide pool applying a rapid sampling technique. Anal Biochem 214:31-37
Van Dyk TK, Rosson RA (1998) Photorhabdus luminescens luxCDABE promoter probe vectors. Methods in Molecular Biology 102:85-95
Van Dyk TK, Ayers BL, Morgan RW, Larossa RA (1998) Constricted flux through the branched-chain amino acid biosynthetic enzyme acetolactate synthase triggers elevated expression of genes regulated by rpoS and internal acidification. J Bacteriol 180:785-792
Van Dyk TK, DeRose EJ, Gonye GE (2001a) LuxArray, a highdensity, genomewide transcription analysis of Escherichia coli using bioluminescent reporter strains. J Bacteriol 183:5496-5505
Van Dyk TK,Wei Y, Hanafey MK, Dolan M, Reeve MJG, Rafalski JA, Rothman-Denes LB, LaRossa RA (2001b) A genomic approach to gene fusion technology. Proc Natl Acad Sci U S A 98:2555-2560
Van Dyk TK, Templeton LJ, Cantera KA, Sharpe PL, Sariaslani FS (2004) Characterization of the Escherichia coli AaeAB efflux pump: A metabolic relief valve? J Bacteriol 186:7196-7204
Varma A, Boesch BW, Palsson BO (1993) Stoichiometric interpretation of Escherichia coli glucose catabolism under various oxygenation rates. Appl Environ Microbiol 59:2465-2473
Visser D, van Zuylen GA, van Dam JC, Eman MR, Proll A, Ras C, Wu L, van Gulik WM, Heijnen JJ (2004) Analysis of in vivo kinetics of glycolysis in aerobic Saccharomyces cerevisiae by application of glucose and ethanol pulses. Biotechnol Bioeng 88:157-167
Weber H, Polen T, Heuveling J, Wendisch VF, Hengge R (2005) Genome-wide analysis of the general stress response network in Escherichia coli: Sigma(S)-dependent genes, promoters, and sigma factor selectivity. J Bacteriol 187:1591-1603
Wolfe AJ (2005) The acetate switch. Microbiol Mol Biol Rev 69:12-50
Xu B, Jahic M, Blomsten G, Enfors SO (1999) Glucose overflow metabolism and mixed-Acid fermentation in aerobic large-scale fed-batch processes with Escherichia coli. Appl Microbiol Biotechnol 51:564-571
Yun HS, Hong J, Lim HC (1996) Regulation of ribosome synthesis in Escherichia coli: Effects of temperature and dilution rate changes. Biotechnol Bioeng 52:615-624
Zanzotto A, Boccazzi P, Gorret N, Van Dyk TK, Sinskey AJ, Jensen KF (2006) In situ measurement of bioluminescence and fluorescence in an integrated microbioreactor. Biotechnol Bioeng 93:40-47