Design of growth-dependent biosensors based on destabilized GFP for the detection of physiological behavior of Escherichia coli in heterogeneous bioreactors

Biotechnology Progress

Volumn 29, Issue 2, 2013, Pages 553-563

  Han, Shanshan ^a   Delvigne, Frank ^b   Brognaux, Alison ^b   Charbon, Gitte E ^a   Sørensen, Søren J ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Destabilized GFP; Escherichia coli; Heterogeneity; Scale down

Indexed keywords

ADDITIONAL EXPERIMENTS; DESTABILIZED GFP; ESCHERICHIA COLI CELLS; FED-BATCH BIOREACTORS; GREEN FLUORESCENT PROTEIN; HETEROGENEITY; SCALE DOWN; SUBSTRATE LIMITATION;

BIOCONVERSION; BIOREACTORS; BIOSENSORS; GLUCOSE; PHYSIOLOGY; STRAIN;

ESCHERICHIA COLI;

GLUCOSE; GREEN FLUORESCENT PROTEIN; OXYGEN;

ARTICLE; BIOREACTOR; CHEMISTRY; ESCHERICHIA COLI; EVALUATION; FERMENTATION; GENETIC PROCEDURES; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; METHODOLOGY; MICROBIOLOGY; REPORTER GENE;

BIOREACTORS; BIOSENSING TECHNIQUES; ESCHERICHIA COLI; FERMENTATION; GENES, REPORTER; GLUCOSE; GREEN FLUORESCENT PROTEINS; OXYGEN;

ESCHERICHIA COLI;

EID: 84875956222     PISSN: 87567938     EISSN: 15206033     Source Type: Journal    
DOI: 10.1002/btpr.1694     Document Type: Article

References (51)

1. Weber H, Polen T, Heuveling J, Wendisch VF, Hengge R. Genome-wide analysis of the general stress response network in Escherichia coli: sigma(S)-dependent genes, promoters, and sigma factor selectivity. J. Bacteriol. 2005;187:1591-1603.
2. 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. Multiple high-throughput analyses monitor the response of E. coli to perturbations. Science. 2007;316:593-597.
3. Lara AR, Galindo E, Ramirez OT, Palomares LA. Living with heterogeneities in bioreactors: understanding the effects of environmental gradients on cells. Mol Biotechnol. 2006;34:355-3581.
4. Aertsen A, Michiels CW. Stress and how bacteria cope with death and survival. Crit. Rev. Microbiol. 2004;30:263-273.
5. Lin HY, Neubauer P. Influence of controlled glucose oscillations on a fed-batch process of recombinant Escherichia coli. J Biotechnol. 2000;79:27-37.
6. Larsson G, Tornkvist M, Wernersson ES, Tragardh C, Noorman H, Enfors SO. Substrate gradients in bioreactors: Origin and consequences. Bioprocess Eng. 1996;14:281-289.
7. Bylund F, Collet E, Enfors SO, Larsson G. Substrate gradient formation in the large-scale bioreactor lowers cell yield and increases by-product formation. Bioprocess Eng. 1998;18:171-180.
8. Enfors SO, Jahic M, Rozkov A, Xu B, Hecker M, Jurgen B, Kruger E, Schweder T, Hamer G, O'Beirne D, Noisommit-Rizzi N, Reuss M, Boone L, Hewitt C, McFarlane C, Nienow A, Kovacs T, Tragardh C, Fuchs L, Revstedt J, Friberg PC, Hjertager B, Blomsten G, Skogman H, Hjort S, Hoeks F, Lin HY, Neubauer P, van der Lans R, Luyben K, Vrabel P, Manelius A. Physiological responses to mixing in large scale bioreactors. J Biotechnol. 2001;85:175-185.
9. Schweder T. Bioprocess monitoring by marker gene analysis. Biotechnol J. 2011;6:926-933.
10. Carlquist M, Fernandes RL, Helmark S, Heins AL, Lundin L, Sorensen SJ, Gernaey KV, Lantz AE. Physiological heterogeneities in microbial populations and implications for physical stress tolerance. Microb Cell Fact. 2012;11.
11. Muller S, Harms H, Bley T. Origin and analysis of microbial population heterogeneity in bioprocesses. Curr Opin Biotechnol. 2010;21:100-113.
12. Delvigne F, Brognaux A, Francis F, Twizere JC, Gorret N, Sorensen SJ, Thonart P. Green fluorescent protein (GFP) leakage from microbial biosensors provides useful information for the evaluation of the scale-down effect. Biotechnol J. 2011;6:968-978.
13. Sorensen SJ, Burmolle M, Hansen LH. Making bio-sense of toxicity: new developments in whole-cell biosensors. Curr Opin Biotechnol. 2006;17:11-16.
14. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC. Green Fluorescent Protein as a Marker for Gene-Expression. Science. 1994;263:802-805.
15. Albano CR, Randers-Eichhorn L, Bentley WE, Rao G. Green fluorescent protein as a real time quantitative reporter of heterologous protein production. Biotechnol Prog. 1998;14:351-354.
16. Chudakov DM, Matz MV, Lukyanov S, Lukyanov KA. Fluorescent proteins and their applications in imaging living cells and tissues. Physiol Rev. 2010;90:1103-1163.
17. Andersen JB, Sternberg C, Poulsen LK, Bjorn SP, Givskov M, Molin S. New unstable variants of green fluorescent protein for studies of transient gene expression in bacteria. Appl Environ Microbiol. 1998;64:2240-2246.
18. Leveau JH, Lindow SE. Predictive and interpretive simulation of green fluorescent protein expression in reporter bacteria. J Bacteriol. 2001;183:6752-6762.
19. Miller WG, Leveau JHJ, Lindow SE. Improved gfp and inaZ broad-host-range promoter-probe vectors. Mol Plant-Microbe Interact. 2000;13:1243-1250.
20. Miller WG, Brandl MT, Quinones B, Lindow SE. Biological sensor for sucrose availability: relative sensitivities of various reporter genes. Appl Environ Microbiol. 2001;67:1308-1317.
21. Delvigne F, Brognaux A, Gorret N, Neubauer P, Delafosse A, Collignon ML, Toye D, Crine M, Thonart P. Characterization of the response of GFP microbial biosensors sensitive to substrate limitation in scale-down bioreactors. Biochem Eng J. 2011;55:131-139.
22. Mateus C, Avery SV. Destabilized green fluorescent protein for monitoring dynamic changes in yeast gene expression with flow cytometry. Yeast. 2000;16:1313-1323.
23. Hackett EA, Esch RK, Maleri S, Errede B. A family of destabilized cyan fluorescent proteins as transcriptional reporters in S-cerevisiae. Yeast. 2006;23:333-349.
24. Avery SV. Microbial cell individuality and the underlying sources of heterogeneity. Nat Rev Microbiol. 2006;4:577-587.
25. Hewitt CJ, Caron GNV, Nienow AW, McFarlane CM. The use of multi-parameter flow cytometry to compare the physiological response of Escherichia coli W3110 to glucose limitation during batch, fed-batch and continuous culture cultivations. J Biotechnol. 1999;75:251-264.
26. Diaz M, Herrero M, Garcia LA, Quiros C. Application of flow cytometry to industrial microbial bioprocesses. Biochem Eng J. 2010;48:385-407.
27. Jin DJ, Cagliero C, Zhou YN. Growth rate regulation in Escherichia coli. FEMS Microbiol Rev. 2012;36:269-287.
28. Gourse RL, Gaal T, Bartlett MS, Appleman JA, Ross W. rRNA transcription and growth rate-dependent regulation of ribosome synthesis in Escherichia coli. Annu Rev Microbiol. 1996;50:645-677.
29. Murray HD, Schneider DA, Gourse RL. Control of rRNA expression by small molecules is dynamic and nonredundant. Mol Cell. 2003;12:125-134.
30. Paul BJ, Barker MM, Ross W, Schneider DA, Webb C, Foster JW, Gourse RL. DksA: a critical component of the transcription initiation machinery that potentiates the regulation of rRNA promoters by ppGpp and the initiating NTP. Cell. 2004;118:311-322.
31. Richins R, Chen W. Effects of FIS overexpression on cell growth, rRNA synthesis, and ribosome content in Escherichia coli. Biotechnol Prog. 2001;17:252-257.
32. L Nilsson HV, E Vijgenboom, C van Drunen, A Vanet and L Bosch FIS-dependent trans activation of stable RNA operons of Escherichia coli under various growth conditions. J Bacteriol. 1992;174:921-929.
33. Zhi H, Wang X, Cabrera JE, Johnson RC, Jin DJ. Fis stabilizes the interaction between RNA polymerase and the ribosomal promoter rrnB P1, leading to transcriptional activation. J Biol Chem. 2003;278:47340-47349.
34. Mallik P, Paul BJ, Rutherford ST, Gourse RL, Osuna R. DksA is required for growth phase-dependent regulation, growth rate-dependent control, and stringent control of fis expression in Escherichia coli. J Bacteriol. 2006;188:5775-5782.
35. Choe LH, Chen W, Lee KH. Proteome analysis of factor for inversion stimulation (Fis) overproduction in Escherichia coli. Electrophoresis. 1999;20:798-805.
36. Schneider R, Travers A, Muskhelishvili G. The expression of the Escherichia coli fis gene is strongly dependent on the superhelical density of DNA. Mol Microbiol. 2000;38:167-175.
37. Neubauer P, Junne, S., Scale-down simulators for metabolic analysis of large-scale bioprocesses. Curr Opin Biotechnol. 2010;21:114-121.
38. Delvigne F, Boxus M, Ingels S, Thonart P. Bioreactor mixing efficiency modulates the activity of a prpoS::GFP reporter gene in E. coli. Microb Cell Fact. 2009;8:15.
39. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951;193:265-275.
40. Dennis PP, Ehrenberg M, Bremer H. Control of rRNA synthesis in Escherichia coli: a systems biology approach. Microbiol Mol Biol Rev. 2004;68:639-668.
41. Lindahl L, Zengel JM. Ribosomal Genes in Escherichia-Coli. Annu Rev Genet. 1986;20:297-326.
42. Kristala Jones Prather SS, Jason Murphy, Michel Chartrain. Industrial scale production of plasmid DNA for vaccine and gene therapy: plasmid design, production, and purification. Enzyme Microb Technol. 2003;33:865-883.
43. Iizuka R, Yamagishi-Shirasaki M, Funatsu T. Kinetic study of de novo chromophore maturation of fluorescent proteins. Anal Biochem. 2011;414:173-178.
44. Ball CA, Osuna R, Ferguson KC, Johnson RC. Dramatic change of fis level upon nutrient upshift in Escherichia coli. J Bacteriol. 1992;174:8043-8056.
45. Bradley MD, Beach MB, Jason de Koning AP, Pratt TS, Osuna R. Effects of Fis on Escherichia coli gene expression during different growth stages. Microbiology. 2007;153:2922-2940.
46. Wick L, Quadroni M, Egli T. Short- and long-term changes in proteome composition and kinetic properties in a culture of Escherichia coli during transition from glucose-excess to glucoselimited growth conditions in continuous culture and vice versa. Environ Microbiol. 2001;3:588-599.
47. Backlund E, Reeks D, Markland K, Weir N, Bowering L, Larsson G. Fedbatch design for periplasmic product retention in Escherichia coli. J Biotechnol. 2008;135:358-365.
48. Shokri A, Sanden AM, Larsson G. Growth rate-dependent changes in Escherichia coli membrane structure and protein leakage. Appl Microbiol Biotechnol. 2002;58:386-392.
49. Shokri A, Larsson G. Characterisation of the Escherichia coli membrane structure and function during fedbatch cultivation. Microb Cell Fact. 2004;3:9.
50. Soini J, Ukkonen K, Neubauer P. Accumulation of amino acids deriving from pyruvate in Escherichia coli W3110 during fed-batch cultivation in a two-compartment scale-down bioreactor. Adv Biosci Biotechnol. 2011;2:336-339.
51. Fritzsch FSO, Dusny C, Frick O, Schmid A. Single-cell analysis in biotechnology, systems biology, and biocatalysis. Annu Rev Chem Biomol Eng. 2012;3:129-155.