Evaluation of cell damage caused by cold sampling and quenching for metabolome analysis

Applied Microbiology and Biotechnology

Volumn 92, Issue 6, 2011, Pages 1261-1274

  Schädel, Friederike ^a   David, Florian ^a   Franco Lara, Ezequiel ^a  

^a TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

Cell leakage; Flow cytometry; Membrane integrity; Propidium iodide; Quenching

Indexed keywords

CELL DAMAGE; CELL LEAKAGE; COLD QUENCHING; COOLING RATES; DAMAGED CELLS; E. COLI; EXPONENTIAL GROWTH PHASE; IN-VIVO; INTRACELLULAR ATP; MEMBRANE INTEGRITY; METABOLOME ANALYSIS; PROPIDIUM IODIDE; SAMPLING TEMPERATURE; SHAKE FLASKS; SINGLE-CELL LEVEL; SINGLECELL ANALYSIS; SOLUTION COMPOSITION;

BOTTLES; CELL MEMBRANES; CYTOLOGY; ESCHERICHIA COLI; FLOW CYTOMETRY;

QUENCHING;

ADENOSINE TRIPHOSPHATE; PROPIDIUM IODIDE;

COLIFORM BACTERIUM; COOLING; FLOW CYTOMETRY; GROWTH CURVE; SAMPLING;

ARTICLE; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERIUM CULTURE; CELL DAMAGE; CELL LEVEL; COLD QUENCHING; COLD SAMPLING; COOLING; ESCHERICHIA COLI; FLOW CYTOMETRY; LOW TEMPERATURE PROCEDURES; METABOLOME; NONHUMAN; OPTICAL DENSITY; SAMPLING; SINGLE CELL ANALYSIS; TEMPERATURE;

ADENOSINE TRIPHOSPHATE; CELL MEMBRANE; COLD TEMPERATURE; ESCHERICHIA COLI; FLOW CYTOMETRY; METABOLOME; MICROBIAL VIABILITY;

ESCHERICHIA COLI;

EID: 82455162431     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-011-3377-1     Document Type: Article

References (71)

1. N Albon JM Sturtevant 1978 Nature of the gel to liquid crystal transition of synthetic phosphatidylcholines Proc Natl Acad Sct USA 75 5 2258 2260 10.1073/pnas.75.5.2258 1:CAS:528:DyaE1cXksFGhsrw%3D (Pubitemid 8349418)
2. L Beney P Gervais 2001 Influence of the fluidity of the membrane on the response of microorganisms to environmental stresses Appl Microbiol Biotechnol 57 34 42 10.1007/s002530100754 1:CAS:528:DC%2BD3MXotVSnurg%3D (Pubitemid 32938349)
3. J Beranová M Jemiola-Rzeminska D Elhottová K Strzalka I Konopásek 2008 Metabolic control of the membrane fluidity in Bacillus subtilis during cold adaptation Biochim Biophys Acta 1778 445 453 10.1016/j.bbamem.2007.11.012
4. CJ Bolten P Kiefer F Letisse J-C Portais C Wittmann 2007 Sampling for metabolome analysis of microorganisms Anal Chem 79 3843 3849 10.1021/ac0623888 1:CAS:528:DC%2BD2sXjvFKgtr0%3D (Pubitemid 46799081)
5. CDK Bottema CA McLean-Bowen LW Parks 1983 Role of sterol structure in the thermotropic behavior of plasma membranes of Saccharomyces cerevisiae Biochim Biophys Acta 734 235 248 10.1016/0005-2736(83)90121-9 1:CAS:528: DyaL3sXlvFSiu7k%3D
6. RJ Britten FT McClure 1962 The amino acid pool in Escherichia coli Bacteriol Rev 26 292 335 1:CAS:528:DyaF3sXosVSgug%3D%3D
7. AB Canelas C Ras A ten Pierick JC van Dam JJ Heijnen WM van Gulik 2008 Leakage-free rapid quenching technique for yeast metabolomics Metabolomics 4 226 239 10.1007/s11306-008-0116-4 1:CAS:528:DC%2BD1cXhtVyis7bO
8. AB Canelas A ten Pierick C Ras RM Seifar JC van Dam WM van Gulik JJ Heijnen 2009 Quantitative evaluation of intracellular metabolite extraction techniques for yeast metabolomics Anal Chem 81 17 7379 7389 10.1021/ac900999t 1:CAS:528:DC%2BD1MXptlelt7Y%3D
9. L Cao-Hoang F Dumont PA Marechal M Le-Thanh P Gervais 2008 Rates of chilling to 0°C: implications for the survival of microorganisms and relationship with membrane fluidity modifications Appl Microbiol Biotechnol 77 1379 1387 10.1007/s00253-007-1279-z 1:CAS:528:DC%2BD1cXhsFSjt7g%3D
10. MA Casadei P Mañas G Niven E Needs BM Mackey 2002 Role of membrane fluidity in pressure resistance of Escherichia coli NCTC 8164 Appl Environ Microbiol 68 12 5965 5972 10.1128/AEM.68.12.5965-5972.2002 1:CAS:528: DC%2BD38Xptlartr8%3D (Pubitemid 36342429)
11. JE Cronan PR Vagelos 1971 Metabolism and function of the membrane phospholipids of Escherichia coli Biochim Biophys Acta 265 25 60
12. W de Koning K van Darn 1992 A method for the determination of changes of gtycolytic metabolites in yeast on a subsecond time scale using extraction at neutral pH Anal Biochem 204 118 123 10.1016/0003-2697(92)90149-2
13. A Delobbe R Haguenauer G Rapoport 1971 Studies on the transport of α-methyl-d-glucoside in Bacillus subtilis 168 Biochimie 53 1015 1021 10.1016/S0300-9084(71)80069-X 1:STN:280:DyaE383hvVWltA%3D%3D
14. M Díaz M Herrero LA García C Quirós 2010 Application of flow cytometry to industrial microbial bioprocesses Biochem Eng J 48 3 385 407 10.1016/j.bej.2009.07.013
15. EZ Drobnis LM Crowe T Berger TJ Anchordoguy JW Overstreet JH Crowe 1993 Cold shock damage is due to lipid phase transitions in cell membranes: a demonstration using sperm as a model J Exp Zool 265 432 437 10.1002/jez. 1402650413 1:CAS:528:DyaK3sXksVKisrc%3D
16. Eze MO (1993) Membrane phase separations, asymetry and implications in the origin of life. Internal report IC/93/381. International Atomic Energy Agency and United Nations Educational Scientific and Cultural Organization, International Centre for Theoretical Physics
17. JP Fay RN Farías 1976 Chilling cells enhances the bactericidal action of fatty acids on Escherichia coli Appl Environ Microbiol 31 2 153 157 1:CAS:528:DyaE28XhtlSrtLo%3D
18. GW Feigenson 2006 Phase behavior of lipid mixtures Nat Chem Biol 2 11 560 563 10.1038/nchembio1106-560 1:CAS:528:DC%2BD28XhtV2gsrzM (Pubitemid 44610335)
19. GW Feigenson 2007 Phase boundaries and biological membranes Annu Rev Biophys Biomol Struct 36 63 77 10.1146/annurev.biophys.36.040306.132721 1:CAS:528:DC%2BD2sXnsVahurw%3D (Pubitemid 46998110)
20. P Granboulan EH Leduc 1967 Ultrastructural cytochemistry of Bacillus subtilis J Ultrastruct Res 20 1-2 111 126 10.1016/S0022-5320(67)80040-6 1:STN:280:DyaE3c3ptl2qtg%3D%3D
21. CWM Haest J de Gier GA van Es AJ Verkleij LLM van Deenen 1972 Fragility of the permeability barrier of Escherichia coli Biochim Biophys Acta 288 43 53 10.1016/0005-2736(72)90221-0 1:CAS:528:DyaE38XlsV2ls7o%3D
22. J Hiller E Franco-Lara D Weuster-Botz 2007 Metabolic profiling of Escherichia coli cultivations: evaluation of extraction and metabolite analysis procedures Biotechnol Lett 29 1169 1178 10.1007/s10529-007-9384-8 1:CAS:528:DC%2BD2sXnt1KitLk%3D (Pubitemid 47035024)
23. AS Janoff A Haug EJ McGroarty 1979 Relationship of growth temperature and thermotropic lipid phase changes in cytoplasmic and outer membranes from Escherichia coli K12 Biochim Biophys Acta 555 56 66 10.1016/0005-2736(79)90071-3 1:CAS:528:DyaE1MXltVGjtb0%3D (Pubitemid 9230617)
24. RI Jepras J Carter SC Pearson FE Paul MJ Wilkinson 1995 Development of a robust flow cytometric assay for determining numbers of viable bacteria Appl Environ Microbiol 61 2696 2701 1:CAS:528:DyaK2MXms1GrsrY%3D
25. KH Jones JA Senft 1985 An improved method to determine cell viability by simultaneous staining with fluorescein diacetate-propidium iodide J Histochem Cytochem 33 77 79 10.1177/33.1.2578146 1:STN:280:DyaL2M%2FotFaltQ%3D%3D (Pubitemid 15189497)
26. PG Jones RA VanBogelen FC Neidhardt 1987 Induction of proteins in response to low temperature in Escherichia coli J Bacteriol 169 2092 2095 1:CAS:528:DyaL2sXktVCjsro%3D (Pubitemid 17081772)
27. K Kato Y Bito 1978 Relationship between bactericidal action of complement and fluidity of cellular membranes Infect Immun 19 1 12 17 1:CAS:528: DyaE1cXhtVehsrg%3D (Pubitemid 8275199)
28. JR Kumita L Jain E Safroneeva GA Woolley 2000 A cystein-free firefly luciferase retains luminescence activity Biochem Biophys Res Comm 267 1 394 397 10.1006/bbrc.1999.1950 1:CAS:528:DC%2BD3cXht1Gkug%3D%3D (Pubitemid 30072562)
29. HC Lange M Eman G van Zuijlen D Visser JC van Dam J Frank MJ Teixeira de Mattos JJ Heijnen 2001 Improved rapid sampling for in vivo kinetics of intracellular metabolites in Saccharomyces cerevisiae Biotechnol Bioeng 75 4 406 415 10.1002/bit.10048 1:CAS:528:DC%2BD3MXosVKisrw%3D (Pubitemid 33043008)
30. C Laroche L Beney PA Marechal P Gervais 2001 The effect of osmotic pressure on the membrane fluidity of Saccharomyces cerevisiae at different physiological temperatures Appl Microbiol Biotechnol 56 249 254 10.1007/s002530000583 1:CAS:528:DC%2BD3MXls1Shtbs%3D (Pubitemid 32661565)
31. IG Leder 1972 Interrelated effects of cold shock and osmotic pressure on the permeability of the Escherichia coli membrane to permease accumulated substrates J Bacteriology 111 1 211 219 1:CAS:528:DyaE38XksFylurc%3D
32. H Link B Anselment D Weuster-Botz 2008 Leakage of adenylates during cold methanol/glycerol quenching of Escherichia coli Metabolomics 4 240 247 10.1007/s11306-008-0114-6 1:CAS:528:DC%2BD1cXhtVyis7nF
33. Mashego M, van Gulik WM, Vinke JL, Heijnen JJ (2003) Critical evaluation of sampling techniques for residual glucose determination in carbon-limited chemostat culture of Saccharomyces cerevisiae. Biotech Bioeng 83(4):395-399. (Pubitemid 36885659)
34. MR Mashego K Rumbold M de Mey E Vandamme W Soetaert JJ Heijnen 2007 Microbial metabolomics: past, present, and future methodologies Biotechnol Lett 29 1 16 10.1007/s10529-006-9218-0 1:CAS:528:DC%2BD28Xht12gsL7I (Pubitemid 44950152)
35. Y Mille L Beney P Gervais 2002 Viability of Escherichia coli after combined osmotic and thermal treatment: a plasma membrane implication Biochim Biophys Acta 1567 41 48 10.1016/S0005-2736(02)00565-5 1:CAS:528: DC%2BD38XpsFWjtrw%3D (Pubitemid 35454045)
36. S Morein A-S Andersson L Rilfors G Lindblom 1996 Wild-type Escherichia coli cells regulate the membrane lipid composition in a "window" between gel and non-lamellar structures J Biol Chem 271 12 6801 6809 10.1074/jbc.271.12.6801 1:CAS:528:DyaK28XhvVyisLc%3D (Pubitemid 26104114)
37. JD Morrisett HJ Pownall RT Plumlee LC Smith ZE Zehner M Esfahani SJ Wakil 1975 Multiple thermotropic phase transitions in Escherichia coli membranes and membrane lipids. A comparison of results obtained by nitroxyl stearate paramagnetic resonance, pyrene excimer fluorescence, and enzyme activity measurements J Biol Chem 250 17 6969 6976 1:CAS:528:DyaE2MXlslCgsb8%3D
38. U Nasution WM van Gulik RJ Kleijn WA van Winden A Proell JJ Heijnen 2006 Measurement of intracellular metabolites of primary metabolism and adenine nucleotides in chemostat cultivated Penicillium chrysogenum Biotechnol Bioeng 94 159 166 10.1002/bit.20842 1:CAS:528:DC%2BD28Xkslejtrk%3D (Pubitemid 43723208)
39. G Nebe-von-Caron RA Badley 1995 Viability assessment of bacteria in mixed populations using flow cytometry J Microscopy 179 55 66 10.1111/j.1365-2818. 1995.tb03612.x
40. G Nebe-von-Caron PJ Stephens CJ Hewitt JR Powell RA Badley 2000 Analysis of bacterial function by multi-colour fluorescence flow cytometry and single cell sorting J Microbiol Methods 42 97 114 10.1016/S0167-7012(00)00181-0 1:CAS:528:DC%2BD3cXms1Sqsbs%3D
41. HC Neu LA Heppel 1965 The release of enzymes from Escherichia coli by osmotic shock and during the formation of spheroplasts J Biol Chem 240 9 3685 3692 1:CAS:528:DyaF2MXksVSiu7s%3D
42. NG Nossal LA Heppel 1966 The release of enzymes by osmotic shock from Escherichia coli in exponential phase J Biol Chem 241 13 3055 3062 1:CAS:528:DyaF28XktFelsr0%3D
43. AH Parola M Ibdah D Gill A Zaritsky 1990 Deviation from homeoviscous adaptation in Escherichia coli membranes Biophys J 57 621 626 10.1016/S0006-3495(90)82578-9 1:CAS:528:DyaK3cXhsFGitr4%3D (Pubitemid 20090198)
44. JR Piperno DL Oxender 1966 Amino acid-binding protein released from Eschericia coli by osmotic shock J Biol Chem 241 23 5732 5734 1:CAS:528:DyaF2sXmtVU%3D
45. C Quirós M Herrero LA García M Díaz 2009 Taking advantage of the flow cytometry technique for improving malolactic starters production Eur Food Res Technol 228 543 552 10.1007/s00217-008-0961-4
46. AS Rudolph JH Crowe LM Crowe 1986 Effects of three stabilizing agents proline, betaine, and trehalose on membrane phospholipids Arch Biochem Biophys 15 134 143 10.1016/0003-9861(86)90197-9 (Pubitemid 16066143)
47. J Saragusty H Gacitua I Rozenboim A Arav 2009 Do physical forces contribute to cryodamage? Biotechnol Bioeng 104 4 719 728 1:CAS:528: DC%2BD1MXhtFOrsbzF
48. AM Scanu C Edelstein 1971 Solubility in aqueous solutions of ethanol of the small molecular weight peptides of the serum very low density and high density lipoproteins: relevance to the recovery problem during delipidation of serum lipoproteins Anal Biochem 44 2 576 588 10.1016/0003-2697(71)90247-8 1:CAS:528:DyaE38Xhs1Sh
49. Schaedel F, Franco-Lara E (2009) Rapid sampling devices for metabolic engineering applications. Applied Microbiology and Biotechnology 83(2):199-208
50. Shapiro HM (2003) Practical flow cytometry, 4th edn. Wiley-Liss, Hoboken
51. L Shi S Günther T Hübschmann LY Wick H Harms S Müller 2007 Limits of propidium iodide as a cell viability indicator for environmental bacteria Cytometry 71 592 598 10.1002/cyto.a.20402 (Pubitemid 47221721)
52. H Simonin L Beney P Gervais 2008 Controlling the membrane fluidity of yeasts during coupled thermal and osmotic treatments Biotechnol Bioeng 100 325 333 10.1002/bit.21749 1:CAS:528:DC%2BD1cXlslCktrk%3D (Pubitemid 351758174)
53. SJ Singer GL Nicolson 1972 The fluid mosaic model of the structure of cell membranes Science 175 23 720 731 10.1126/science.175.4023.720 1:CAS:528:DyaE38Xht1eisbg%3D
54. J Spura LC Reimer P Wieloch K Schreiber S Buchinger D Schomburg 2009 A method for enzyme quenching in microbial metabolome analysis successfully applied to Gram-positive and Gram-negative bacteria and yeast Anal Biochem 394 192 201 10.1016/j.ab.2009.07.016 1:CAS:528:DC%2BD1MXhtFams7fK
55. D Sung H Kang 1998 The N-terminal amino acid sequences of firefly luciferase are important for the stability of the enzyme Photochem Photobiol 68 5 749 753 10.1111/j.1751-1097.1998.tb02540.x 1:CAS:528:DyaK1cXns12nurs%3D (Pubitemid 128472306)
56. A Svarachorn T Tsuchido A Shinmyo M Takano 1991 Autolysis of Bacillus subtilis induced by low temperature J Ferm Bioeng 71 4 281 283 10.1016/0922-338X(91)90283-M 1:CAS:528:DyaK3MXisVCiurs%3D
57. JM Sztein K Noble JS Farley LE Mobraaten 2001 Comparison of permeating and nonpermeating cryoprotectants for mouse sperm cryopreservation Cryobiol 42 1 28 39 10.1006/cryo.2001.2300 1:CAS:528:DC%2BD3MXjt1Wgsb4%3D (Pubitemid 34169360)
58. H Taymaz-Nikerel M de Mey C Ras A ten Pierick RM Seifar JC van Dam JJ Heijnen WM van Gulik 2009 Development and application of a differential method for reliable metabolome analysis in Escherichia coli Anal Biochem 386 1 9 19 10.1016/j.ab.2008.11.018 1:CAS:528:DC%2BD1MXhtFenur8%3D
59. U Theobald W Mailinger M Reuss M Rizzi 1993 In vivo analysis of glucose-induced fast changes in yeast adenine nucleotide pool applying a rapid sampling technique Anal Biochem 214 1 31 37 10.1006/abio.1993.1452 1:CAS:528:DyaK3sXms1Gltb4%3D (Pubitemid 23300349)
60. HA Thieringer PG Jones M Inouye 1998 Cold shock and adaptation Bioessays 20 49 57 10.1002/(SICI)1521-1878(199801)20:1<49::AID-BIES8>3.0.CO;2-N 1:STN:280:DyaK1c7msVOqug%3D%3D (Pubitemid 28111331)
61. M Tibbett F Sanders J Cairney 2002 Low-temperature-induced changes in trehalose, mannitol and arabitol associated with enhanced tolerance to freezing in ectomycorrhizal basidiomycetes (Hebeloma spp.) Mycorrhiza 12 5 249 255 10.1007/s00572-002-0183-8 1:CAS:528:DC%2BD38XpsFKhsL4%3D (Pubitemid 36053080)
62. T Tsuchido T Nishino Y Kato M Takano 1995 Involvement of membrane lipids in cold shock-induced autolysis of Bacillus subtilis cells Biosci Biotechnol Biochem 59 1636 1640 10.1271/bbb.59.1636 1:CAS:528:DyaK2MXosFShsbk%3D
63. G van Meer DR Voelker GW Feigenson 2008 Membrane lipids: where they are and how they behave Mol Cell Biol 9 112 124 (Pubitemid 351158912)
64. SG Villas-Boas P Bruheim 2007 Cold glycerol-saline: the promising quenching solution for accurate intracellular metabolite analysis of microbial cells Anal Biochem 370 87 97 10.1016/j.ab.2007.06.028 1:CAS:528: DC%2BD2sXhtVOmur3I (Pubitemid 47404490)
65. Villas-Bôas SG, Nielsen J, Smedsgaard J, Hansen MAE, Roessner-Tunali U (2007) Metabolome analysis: an introduction. Wiley, Hoboken
66. RJ Wargel CA Shadur FC Neuhaus 1970 Mechanisms of d-cycloserine action: transport systems for d-alanine, d-cycloserine, l-alanine and glycin J Bacteriol 103 3 778 788 1:CAS:528:DyaE3cXkvVCqtL0%3D
67. M Wellerdiek D Winterhoff W Reule J Brandner M Oldiges 2009 Metabolic quenching of Corynebacterium glutamicum: efficiency of methods and impact of cold shock Bioprocess Biosys Eng 32 5 581 592 10.1007/s00449-008-0280-y 1:CAS:528:DC%2BD1MXovVOiurs%3D
68. Weuster-Botz D (1999) Die Rolle der Reaktionstechnik in der mikrobiellen Verfahrensentwicklung. Forschungszentrums Jülich/Life Sciences 2. ISBN-10: 3893362452; ISBN-13: 978-3893362455; ISSN: 1433-5549
69. C Wittmann JO Kromer P Kiefer T Binz E Heinzle 2004 Impact of the cold shock phenomenon on quantification of intracellular metabolites in bacteria Anal Biochem 327 135 139 10.1016/j.ab.2004.01.002 1:CAS:528:DC%2BD2cXitFKht7g%3D (Pubitemid 38367993)
70. K Yamanaka 1999 Cold shock response in Escherichia coli J Mol Microbiol Biotechnol 1 2 193 202 1:CAS:528:DyaK1MXnvF2htr8%3D (Pubitemid 129491941)
71. L Zamai E Falcieri G Marhefka M Vitale 1996 Supravital exposure to propidium iodide identifies apoptotic cells in the absence of nucleosomal DNA fragmentation Cytometry 23 303 311 10.1002/(SICI)1097-0320(19960401)23:4<303: :AID-CYTO6>3.0.CO;2-H 1:CAS:528:DyaK28Xis1OktrY%3D (Pubitemid 26129150)