Physiological, biomass elemental composition and proteomic analyses of Escherichia coli ammoniumlimited chemostat growth, and comparison with iron- and glucose-limited chemostat growth

Microbiology (United Kingdom)

Volumn 161, Issue 8, 2015, Pages 1659-1670

  Folsom, James Patrick ^a,b   Carlson, Ross P ^a,b  

^a Idaho National Laboratory   (United States)

^b MONTANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; ADENOSINE TRIPHOSPHATE; AMMONIA; BACTERIAL ENZYME; CARBON; FORMIC ACID; GLUCOSE; GLYCOLYTIC ENZYME; IRON; LACTIC ACID; NITROGEN; PROTEOME; TRICARBOXYLIC ACID; AMMONIUM DERIVATIVE; CULTURE MEDIUM; ESCHERICHIA COLI PROTEIN;

ARTICLE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM CULTURE; BIOCHEMICAL COMPOSITION; CARBON METABOLISM; CHEMOSTAT; CITRIC ACID CYCLE; CONTROLLED STUDY; DILUTION; ENZYME METABOLISM; ESCHERICHIA COLI; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLYCOLYSIS; MICROBIAL BIOMASS; NONHUMAN; NUTRIENT CONTENT; NUTRIENT LIMITATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEOMICS; STOICHIOMETRY; CHEMISTRY; CULTURE MEDIUM; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

ESCHERICHIA COLI;

AMMONIUM COMPOUNDS; CITRIC ACID CYCLE; CULTURE MEDIA; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GLUCOSE; IRON; PROTEOMICS;

EID: 85042579182     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.000118     Document Type: Article

References (61)

1. Abdul-Tehrani, H., Hudson, A. J., Chang, Y. S., Timms, A. R., Hawkins, C., Williams, J. M., Harrison, P. M., Guest, J. R. & Andrews, S. C. (1999). Ferritin mutants of Escherichia coli are iron deficient and growth impaired, and fur mutants are iron deficient. J Bacteriol 181, 1415-1428.
2. Alexeeva, S., de Kort, B., Sawers, G., Hellingwerf, K. J. & de Mattos, M. J. T. (2000). Effects of limited aeration and of the ArcAB system on intermediary pyruvate catabolism in Escherichia coli. J Bacteriol 182, 4934-4940.
3. Bauer, S. & Ziv, E. (1976). Dense growth of aerobic bacteria in a bench-scale fermentor. Biotechnol Bioeng 18, 81-94.
4. Becker, A., Fritz-Wolf, K., Kabsch, W., Knappe, J., Schultz, S. & Volker Wagner, A. F. (1999). Structure and mechanism of the glycyl radical enzyme pyruvate formate-lyase. Nat Struct Biol 6, 969-975.
5. Bloom, A. J., Chapin, F. S. & Mooney, H. A. (1985). Resource limitation in plants-an economic analogy. Annu Rev Ecol Evol Syst 16, 363-392.
6. Brauer, M. J., Yuan, J., Bennett, B. D., Lu, W., Kimball, E., Botstein, D. & Rabinowitz, J. D. (2006). Conservation of the metabolomic response to starvation across two divergent microbes. Proc Natl Acad Sci U S A 103, 19302-19307.
7. Bull, A. T. (2010). The renaissance of continuous culture in the postgenomics age. J Ind Microbiol Biotechnol 37, 993-1021.
8. Carlson, R. P. (2007). Metabolic systems cost-benefit analysis for interpreting network structure and regulation. Bioinformatics 23, 1258-1264.
9. Carlson, R. P. (2009). Decomposition of complex microbial behaviors into resource-based stress responses. Bioinformatics 25, 90-97.
10. Carlson, R. & Srienc, F. (2004). Fundamental Escherichia coli biochemical pathways for biomass and energy production: creation of overall flux states. Biotechnol Bioeng 86, 149-162.
11. Carlson, R. P. & Taffs, R. L. (2010). Molecular-level tradeoffs and metabolic adaptation to simultaneous stressors. Curr Opin Biotechnol 21, 670-676.
12. Castan, A. & Enfors, S. O. (2002). Formate accumulation due to DNA release in aerobic cultivations of Escherichia coli. Biotechnol Bioeng 77, 324-328.
13. Chevalier, F. (2010). Highlights on the capacities of "gel-based" proteomics. Proteome Sci 8, 23.
14. Chrzanowski, T. H. & Grover, J. P. (2008). Element content of Pseudomonas fluorescens varies with growth rate and temperature: a replicated chemostat study addressing ecological stoichiometry. Limnol Oceanogr 53, 1242-1251.
15. Clark, D. P. (1989). The fermentation pathways of Escherichia coli. FEMS Microbiol Rev 5, 223-234.
16. Cordier, J.-L., Butsch, B., Birou, B. & Stockar, U. (1987). The relationship between elemental composition and heat of combustion of microbial biomass. Appl Microbiol Biotechnol 25, 305-312.
17. Cotner, J. B., Makino, W. & Biddanda, B. A. (2006). Temperature affects stoichiometry and biochemical composition of Escherichia coli. Microb Ecol 52, 26-33.
18. De Maeseneire, S. L., De Mey, M., Vandedrinck, S. & Vandamme, E. J. (2006). Metabolic characterisation of E. coli citrate synthase and phosphoenolpyruvate carboxylase mutants in aerobic cultures. Biotechnol Lett 28, 1945-1953.
19. Del Don, C., Hanselmann, K. W., Peduzzi, R. & Bachofen, R. (1994). Biomass composition and methods for the determination of metabolic reserve polymers in phototrophic sulfur bacteria. Aquat Sci 56, 1-15.
20. Dratz, E. A. & Grieco, P. (2009). Novel optical labeling molecules in proteomics and other biological analyses. World Patent 2009/005871-A.
21. Egli, T. (1991). On multiple-nutrient-limited growth ofmicroorganisms, with special reference to dual limitation by carbon and nitrogen substrates. Antonie van Leeuwenhoek 60, 225-234.
22. Fischer, E. & Sauer, U. (2003). A novel metabolic cycle catalyzes glucose oxidation and anaplerosis in hungry Escherichia coli. J Biol Chem 278, 46446-46451.
23. Folsom, J. P., Parker, A. E. & Carlson, R. P. (2014). Physiological and proteomic analysis of Escherichia coli iron-limited chemostat growth. J Bacteriol 196, 2748-2761.
24. Heldal, M., Norland, S., Fagerbakke, K., Thingstad, F. & Bratbak, G. (1996). The elemental composition of bacteria: a signature of growth conditions? Mar Pollut Bull 33, 3-9.
25. Ho, K. P. & Payne, W. J. (1979). Assimilation efficiency and energy contents of prototrophic bacteria. Biotechnol Bioeng 21, 787-802.
26. Holme, T., Westöö, G., Svennerholm, L., Magné li, A., Magné li, A., Pestmalis, H. & Åsbrink, S. (1957). Continuous culture studies on glycogen synthesis in Escherichia coli B. Acta Chem Scand 11, 763-775.
27. Hua, Q., Yang, C., Baba, T., Mori, H. & Shimizu, K. (2003). Responses of the central metabolism in Escherichia coli to phosphoglucose isomerase and glucose-6-phosphate dehydrogenase knockouts. J Bacteriol 185, 7053-7067.
28. Hua, Q., Yang, C., Oshima, T., Mori, H. & Shimizu, K. (2004). Analysis of gene expression in Escherichia coli in response to changes of growth-limiting nutrient in chemostat cultures. Appl Environ Microbiol 70, 2354-2366.
29. Hudson, A. J., Andrews, S. C., Hawkins, C., Williams, J. M., Izuhara, M., Meldrum, F. C., Mann, S., Harrison, P. M. & Guest, J. R. (1993). Overproduction, purification and characterization of the Escherichia coli ferritin. Eur J Biochem 218, 985-995.
30. Ihssen, J. & Egli, T. (2004). Specific growth rate and not cell density controls the general stress response in Escherichia coli. Microbiology 150, 1637-1648.
31. Keshavarz, T. & Roy, I. (2010). Polyhydroxyalkanoates: bioplastics with a green agenda. Curr Opin Microbiol 13, 321-326.
32. Kussell, E. & Leibler, S. (2005). Phenotypic diversity, population growth, and information in fluctuating environments. Science 309, 2075-2078.
33. Kussell, E., Kishony, R., Balaban, N. Q. & Leibler, S. (2005). Bacterial persistence: a model of survival in changing environments. Genetics 169, 1807-1814.
34. Law, R. (1979). Optimal life histories under age-specific predation. Am Nat 114, 399-417.
35. Liu, X. & Ferenci, T. (1998). Regulation of porin-mediated outer membrane permeability by nutrient limitation in Escherichia coli. J Bacteriol 180, 3917-3922.
36. Miller, T. E., Burns, J. H., Munguia, P., Walters, E. L., Kneitel, J. M., Richards, P. M., Mouquet, N. & Buckley, H. L. (2005). A critical review of twenty years' use of the resource-ratio theory. Am Nat 165, 439-448.
37. Molenaar, D., vanBerlo, R., deRidder, D. & Teusink, B. (2009). Shifts in growth strategies reflect tradeoffs in cellular economics. Mol Syst Biol 5, 323.
38. Monod, J. (1950). [The continuous culture technique: theory and applications]. Ann Inst Pasteur (Paris) 79, 390 (in French).
39. Moreau, P. L. (2007). The lysine decarboxylase CadA protects Escherichia coli starved of phosphate against fermentation acids. J Bacteriol 189, 2249-2261.
40. Nanchen, A., Schicker, A. & Sauer, U. (2006). Nonlinear dependency of intracellular fluxes on growth rate in miniaturized continuous cultures of Escherichia coli. Appl Environ Microbiol 72, 1164-1172.
41. Natarajan, A. & Srienc, F. (2000). Glucose uptake rates of single E. coli cells grown in glucose-limited chemostat cultures. J Microbiol Methods 42, 87-96.
42. Neijssel, O. M., Teixeira de Mattos, M. J. & Tempest, D. W. (1996). Growth yield and energy distribution. In Escherichia coli and Salmonella: Cellular and Molecular Biology, pp. 1683-1692. Edited by F. C. Neidhardt. Washington, DC: American Society for Microbiology.
43. Novick, A. & Szilard, L. (1950). Description of the chemostat. Science 112, 715-716.
44. Pickett, A. M., Bazin, M. J. & Topiwala, H. H. (1979). Growth and composition of Escherichia coli subjected to square-wave perturbations in nutrient supply: effect of varying frequencies. Biotechnol Bioeng 21, 1043-1055.
45. Pirt, S. J. (1975). Principles of Microbe Cultivation. Oxford: Blackwell Scientific.
46. Pirt, S. J. (1982). Maintenance energy: a general model for energylimited and energy-sufficient growth. Arch Microbiol 133, 300-302.
47. Roels, J. A. (1980). Application of macroscopic principles to microbial metabolism. Biotechnol Bioeng 22, 2457-2514.
48. Sauer, U., Lasko, D. R., Fiaux, J., Hochuli, M., Glaser, R., Szyperski, T., Wüthrich, K. & Bailey, J. E. (1999). Metabolic flux ratio analysis of genetic and environmental modulations of Escherichia coli central carbon metabolism. J Bacteriol 181, 6679-6688.
49. Schliep, M., Ryall, B. & Ferenci, T. (2012). The identification of global patterns and unique signatures of proteins across 14 environments using outer membrane proteomics of bacteria. Mol Biosyst 8, 3017-3027.
50. Scott, J. T., Cotner, J. B. & Lapara, T. M. (2012). Variable stoichiometry and homeostatic regulation of bacterial biomass elemental composition. Front Microbiol 3, 42.
51. Searle, P. L. (1984). The Berthelot or indophenol reaction and its use in the analytical chemistry of nitrogen: a review. Analyst (Lond) 109, 549-568.
52. Senior, P. J. (1975). Regulation of nitrogen metabolism in Escherichia coli and Klebsiella aerogenes: studies with the continuous-culture technique. J Bacteriol 123, 407-418.
53. Shipman, M., Lubick, K., Fouchard, D., Guram, R., Grieco, P., Jutila, M. & Dratz, E. A. (2012). Proteomic and systems biology analysis of monocytes exposed to securinine, a GABAA receptor antagonist and immune adjuvant. PLoS One 7, e41278.
54. Simonds, S., Grover, J. P. & Chrzanowski, T. H. (2010). Element content of Ochromonas danica: a replicated chemostat study controlling the growth rate and temperature. FEMS Microbiol Ecol 74, 346-352.
55. Sterner, R. W. & Elser, J. J. (2002). Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere. Princeton, NJ: Princeton University Press.
56. Stieg, S. (2005). 4500-NH3 F. Phenate method. In Standard Methods for the Examination of Water and Wastewater, pp. 4-114. Edited by A. D. Eaton, L. S. Clesceri, E. W. Rice, A. E. Greenberg & M. A. H. Franson. Washington, DC: American Public Health Association/American Water Works Association/Water Environment Federation.
57. Sukmarini, L. & Shimizu, K. (2010). Metabolic regulation of Escherichia coli and its glnG and zwf mutants under nitrogen limitation. Biochem Eng J 48, 230-236.
58. Tilman, D. (1982). Resource Competition and Community Structure., Princeton, NJ: Princeton University Press.
59. Wagner, A. F., Schultz, S., Bomke, J., Pils, T., Lehmann, W. D. & Knappe, J. (2001). YfiD of Escherichia coli and Y06I of bacteriophage T4 as autonomous glycyl radical cofactors reconstituting the catalytic center of oxygen-fragmented pyruvate formate-lyase. Biochem Biophys Res Commun 285, 456-462.
60. Wang, C. C. & Newton, A. (1969). Iron transport in Escherichia coli: roles of energy-dependent uptake and 2, 3-dihydroxybenzoylserine. J Bacteriol 98, 1142-1150.
61. Zhu, J., Shalel-Levanon, S., Bennett, G. & San, K. Y. (2007). The YfiD protein contributes to the pyruvate formate-lyase flux in an Escherichia coli arcA mutant strain. Biotechnol Bioeng 97, 138-143.