Bacterial growth laws reflect the evolutionary importance of energy efficiency

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 2, 2015, Pages 406-411

  Maitra, Arijit ^a   Dill, Ken A ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

Bacterial metabolism; Energy efficiency; Fitness landscape; Growth laws; Yield

Indexed keywords

CELL PROTEIN; RIBOSOME PROTEIN; ESCHERICHIA COLI PROTEIN;

ARTICLE; BACTERIAL GROWTH; CELL DENSITY; CELL GROWTH; ENERGY; ENERGY BALANCE; ENERGY COST; ENERGY METABOLISM; ESCHERICHIA COLI; EVOLUTION; GROWTH RATE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PRODUCTIVITY; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; RIBOSOME; STEADY STATE; BACTERIUM; BIOLOGICAL MODEL; BIOSYNTHESIS; GROWTH, DEVELOPMENT AND AGING; KINETICS; METABOLISM; NONRIBOSOMAL PEPTIDE SYNTHESIS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

BACTERIA; BIOLOGICAL EVOLUTION; ENERGY METABOLISM; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; KINETICS; MODELS, BIOLOGICAL; PEPTIDE BIOSYNTHESIS, NUCLEIC ACID-INDEPENDENT; RIBOSOMAL PROTEINS; RIBOSOMES;

EID: 84949114770     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1421138111     Document Type: Article

References (47)

1. Monod J (1949) The growth of bacterial cultures. Annu Rev Microbiol 3:371-394.
2. Hinshelwood CN (1952) On the chemical kinetics of autosynthetic systems. J Chem Soc 745-755.
3. Ehrenberg M, Kurland CG (1984) Costs of accuracy determined by a maximal growth rate constraint. Q Rev Biophys 17(1):45-82.
4. Koch AL (1988) Why can't a cell grow infinitely fast? Can J Microbiol 34(4):421-426.
5. Cox RA (2004) Quantitative relationships for specific growth rates and macromolecular compositions of Mycobacterium tuberculosis, Streptomyces coelicolor A3(2) and Escherichia coli B/r: An integrative theoretical approach. Microbiology 150(Pt 5): 1413-1426.
6. Bremer H, Dennis P (1996) Modulation of chemical composition and other parameters of the cell by growth rate. Escherichia coli and Salmonella, ed Neidhardt FC (American Society for Microbiology Press, Washington, DC).
7. Phillips R, Milo R (2009) A feeling for the numbers in biology. Proc Natl Acad Sci USA 106(51):21465-21471.
8. Youk H, van Oudenaarden A (2009) Growth landscape formed by perception and import of glucose in yeast. Nature 462(7275):875-879.
9. Klumpp S, Zhang Z, Hwa T (2009) Growth rate-dependent global effects on gene expression in bacteria. Cell 139(7):1366-1375.
10. Scott M, Gunderson CW, Mateescu EM, Zhang Z, Hwa T (2010) Interdependence of cell growth and gene expression: Origins and consequences. Science 330(6007):1099-1102.
11. Scott M, Hwa T (2011) Bacterial growth laws and their applications. Curr Opin Biotechnol 22(4):559-565.
12. Scott M, Klumpp S, Mateescu EM, Hwa T (2014) Emergence of robust growth laws from optimal regulation of ribosome synthesis. Mol Syst Biol 10:747.
13. Orr HA (2009) Fitness and its role in evolutionary genetics. Nat Rev Genet 10(8): 531-539.
14. Klumpp S, Scott M, Pedersen S, Hwa T (2013) Molecular crowding limits translation and cell growth. Proc Natl Acad Sci USA 110(42):16754-16759.
15. Molenaar D, van Berlo R, de Ridder D, Teusink B (2009) Shifts in growth strategies reflect tradeoffs in cellular economics. Mol Syst Biol 5:323.
16. Neidhardt F, Ingraham J, SchaechterM (1990) Physiology of the Bacterial Cell (Sinauer Associates, Sunderland, MA).
17. Stouthamer AH, Bettenhaussen C (1973) Utilization of energy for growth and maintenance in continuous and batch cultures of microorganisms: A reevaluation of the method for the determination of ATP production by measuring molar growth yields. Biochimica et Biophysica Acta-Reviews on Bioenergetics 301(1):53-70.
18. Tempest DW, Neijssel OM (1984) The status of YATP and maintenance energy as biologically interpretable phenomena. Annu Rev Microbiol 38:459-486.
19. Dekel E, Alon U (2005) Optimality and evolutionary tuning of the expression level of a protein. Nature 436(7050):588-592.
20. Stoebel DM, Dean AM, Dykhuizen DE (2008) The cost of expression of Escherichia coli lac operon proteins is in the process, not in the products. Genetics 178(3):1653-1660.
21. Trötschel C, Albaum SP, Poetsch A (2013) Proteome turnover in bacteria: Current status for Corynebacterium glutamicum and related bacteria. Microb Biotechnol 6(6):708-719.
22. Dressaire C, et al. (2009) Transcriptome and proteome exploration to model translation efficiency and protein stability in Lactococcus lactis. PLOS Comput Biol 5(12): e1000606.
23. Belle A, Tanay A, Bitincka L, Shamir R, O'Shea EK (2006) Quantification of protein halflives in the budding yeast proteome. Proc Natl Acad Sci USA 103(35):13004-13009.
24. Eden E, et al. (2011) Proteome half-life dynamics in living human cells. Science 331(6018): 764-768.
25. Zundel MA, Basturea GN, Deutscher MP (2009) Initiation of ribosome degradation during starvation in Escherichia coli. RNA 15(5):977-983.
26. Jewett MC, Miller ML, Chen Y, Swartz JR (2009) Continued protein synthesis at low [ATP] and [GTP] enables cell adaptation during energy limitation. J Bacteriol 191(3):1083-1091.
27. Westerhoff HV, Hellingwerf KJ, Van Dam K (1983) Thermodynamic efficiency of microbial growth is low but optimal for maximal growth rate. Proc Natl Acad Sci USA 80(1):305-309.
28. Schuetz R, Zamboni N, Zampieri M, Heinemann M, Sauer U (2012) Multidimensional optimality of microbial metabolism. Science 336(6081):601-604.
29. DeLong JP, Okie JG, Moses ME, Sibly RM, Brown JH (2010) Shifts in metabolic scaling, production, and efficiency across major evolutionary transitions of life. Proc Natl Acad Sci USA 107(29):12941-12945.
30. Farmer IS, Jones CW (1976) The energetics of Escherichia coli during aerobic growth in continuous culture. Eur J Biochem 67(1):115-122.
31. Kayser A, Weber J, Hecht V, Rinas U (2005) Metabolic flux analysis of Escherichia coli in glucose-limited continuous culture. I. Growth-rate-dependent metabolic efficiency at steady state. Microbiology 151(Pt 3):693-706.
32. Schaechter M, Maaloe O, Kjeldgaard NO (1958) Dependency on medium and temperature of cell size and chemical composition during balanced grown of Salmonella typhimurium. J Gen Microbiol 19(3):592-606.
33. Zaslaver A, et al. (2009) Invariant distribution of promoter activities in Escherichia coli. PLOS Comput Biol 5(10):e1000545.
34. Dalbow DG, Young R (1975) Synthesis time of galactosidase in Escherichia coli B/r as a function of growth rate. Biochem J 150(1):13-20.
35. Kepes A, Beguin S (1966) Peptide chain initiation and growth in the induced synthesis of beta-galactosidase. Biochim Biophys Acta 123(3):546-560.
36. Coffman RL, Norris TE, Koch AL (1971) Chain elongation rate of messenger and polypeptides in slowly growing Escherichia coli. J Mol Biol 60(1):1-19.
37. Morris DR, Hansen MT (1973) Influence of polyamine limitation on the chain growth rates of beta-galactosidase and of its messenger ribonucleic acid. J Bacteriol 116(2):588-592.
38. Schleif R, Hess W, Finkelstein S, Ellis D (1973) Induction kinetics of the L-arabinose operon of Escherichia coli. J Bacteriol 115(1):9-14.
39. Young R, Bremer H (1976) Polypeptide-chain-elongation rate in Escherichia coli B/r as a function of growth rate. Biochem J 160(2):185-194.
40. Koch AL (1980) The inefficiency of ribosomes functioning in Escherichia coli growing at moderate rates. J Gen Microbiol 116(1):165-171.
41. Pedersen S (1984) Escherichia coli ribosomes translate in vivo with variable rate. EMBO J 3(12):2895-2898.
42. Neijssel O, de Mattos MT, Tempest D (1996) Growth yield and energy distribution. Escherichia coli and Salmonella, ed Neidhardt FC (ASM Press, Washington, DC).
43. Vemuri GN, Altman E, Sangurdekar DP, Khodursky AB, Eiteman MA (2006) Overflow metabolism in Escherichia coli during steady-state growth: transcriptional regulation and effect of the redox ratio. Appl Environ Microbiol 72(5):3653-3661.
44. Forchhammer J, Lindahl L (1971) Growth rate of polypeptide chains as a function of the cell growth rate in a mutant of Escherichia coli 15. J Mol Biol 55(3):563-568.
45. Ishii N, et al. (2006) Multiple high-throughput analyses moniter the response of the E. coli to perturbations. Science 316(5824):593-597.
46. Bakshi S, Siryaporn A, Goulian M, Weisshaar JC (2012) Superresolution imaging of ribosomes and RNA polymerase in live Escherichia coli cells. Mol Microbiol 85(1):21-38.
47. Zhang J (2000) Protein-length distributions for the three domains of life. Trends Genet 16(3):107-109.