Ribosome Abundance Control in Prokaryotes.
Mathematical model
Ribosome
Ribosome abundance control
Journal
Bulletin of mathematical biology
ISSN: 1522-9602
Titre abrégé: Bull Math Biol
Pays: United States
ID NLM: 0401404
Informations de publication
Date de publication:
20 10 2023
20 10 2023
Historique:
received:
01
05
2023
accepted:
06
09
2023
medline:
2
11
2023
pubmed:
20
10
2023
entrez:
20
10
2023
Statut:
epublish
Résumé
Cell growth is an essential phenotype of any unicellular organism and it crucially depends on precise control of protein synthesis. We construct a model of the feedback mechanisms that regulate abundance of ribosomes in E. coli, a prototypical prokaryotic organism. Since ribosomes are needed to produce more ribosomes, the model includes a positive feedback loop central to the control of cell growth. Our analysis of the model shows that there can be only two coexisting equilibrium states across all 23 parameters. This precludes the existence of hysteresis, suggesting that the ribosome abundance changes continuously with parameters. These states are related by a transcritical bifurcation, and we provide an analytic formula for parameters that admit either state.
Identifiants
pubmed: 37861893
doi: 10.1007/s11538-023-01212-w
pii: 10.1007/s11538-023-01212-w
doi:
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
119Informations de copyright
© 2023. The Author(s), under exclusive licence to Society for Mathematical Biology.
Références
Boutte CC, Crosson S (2013) Bacterial lifestyle shapes the regulation of stringent response activation. Trends Microbiol 21(4):174–180
doi: 10.1016/j.tim.2013.01.002
Brackley CA, Romano MC, Thiel M (2010) Slow sites in an exclusion process with limited resources. Phys Rev E 82:051920. https://doi.org/10.1103/PhysRevE.82.051920
doi: 10.1103/PhysRevE.82.051920
Bremer H, Dennis PP (1996) Modulation of chemical composition and other parameters of the cell by growth rate. In: Neidhardt EA (ed) Escherichia Coli and salmonella typhimurium: cellular and molecular biology. Chap. 97
Buckstein M, He J, Rubin H (2008) Characterization of nucleotide pools as a function of physiological state in Escherichia coli. J Bacteriol 190(2):718–726
doi: 10.1128/JB.01020-07
Chen S, Sperling E, Silverman J, Davis J, Williamson J (2012) Measuring the dynamics of E. coli ribosome biogenesis using pulse-labeling and quantitative mass spectrometry. Mol Biosyst 8:3325–3334
doi: 10.1039/c2mb25310k
Chen H, Shiroguchi K, Ge H, Xie X (2015) Genome-wide study of mRNA degradation and transcript elongation in Escherichia coli. Mol Syst Biol 11(781)
Condon C, French S, Squires C, Squires CL (1993) Depletion of functional ribosomal RNA operons in Escherichia coli causes increased expression of the remaining intact copies. EMBO J 12(11):4305–4315
doi: 10.1002/j.1460-2075.1993.tb06115.x
Condon C, Liveris D, Squires C, Schwartz I, Squires CL (1995) rRNA operon multiplicity in Escherichia coli and the physiological implications of rrn inactivation. J Bacteriol 177(14):4152–4156
doi: 10.1128/jb.177.14.4152-4156.1995
Davis L, Gedeon T, Gedeon J, Thorenson J (2013) A traffic flow model for bio-polymerization processes. J Math Biol. https://doi.org/10.1007/s00285-013-0651-0
doi: 10.1007/s00285-013-0651-0
Davis J, Willamson J (2017) Structure and dynamics of bacterial ribosome biogenesis. Philos Trans B 372(20160181)
Elf J, Ehrenberg M (2005) Near-critical behavior of aminoacyl-tRNA pools in E. coli at rate-limiting supply of amino acids. Biophys J. 88(1): 132–146 (2005). https://doi.org/10.1529/biophysj.104.051383
Erickson DW, Schink SJ, Patsalo V, Williamson JR, Gerland U, Hwa T (2017) A global resource allocation strategy governs growth transition kinetics of Escherichia coli. Nature 551(7678):119–123
doi: 10.1038/nature24299
Gaal T, Bartlett MS, Ross W, Turnbough CL, Gourse RL (1997) Transcription regulation by initiating NTP concentration: rRNA synthesis in bacteria. Science 278(5346):2092–2097
doi: 10.1126/science.278.5346.2092
Gale E, Epps H (1942) The effect of the pH of the medium during growth on the enzymic activities of bacteria (Escherichia coli and Micrococcus lysodeikticus) and the biological significance of the changes produced. Biochem J 36(7–9):600–618. https://doi.org/10.1042/bj0360600
doi: 10.1042/bj0360600
Gallant J, Margasin G, Finch B (1972) On the turnover of ppGpp in Escherischia coli. J Biol Chem 247(19):6055–6058
doi: 10.1016/S0021-9258(19)44762-5
Griffiths AJF, Gelbart WM, Miller JH, Lewontin RC (1999) Modern genetic analysis. W. H. Freeman and Co., New York
Gyorfy Z, Draskovits G, Vernyik V, Blattner FF, Gaal T, Posfai G (2015) Engineered ribosomal RNA operon copy-number variants of E. coli reveal the evolutionary trade-offs shaping rRNA operon number. Nucleic Acid Res
Hauryliuk V, Atkinson GC, Murakami KS, Tenson T, Gerdes K (2015) Recent functional insights into the role of (p)ppGpp in bacterial physiology. Nat Rev Microbiol 13:298–309
doi: 10.1038/nrmicro3448
Keener J, Sneyd J (2008) Mathematical physiology I: cellular physiology, 2nd edn. Springer, New York, NY
Klumpp S, Hwa T (2008) Stochasticity and traffic jams in the transcription of ribosomal RNA: intriguing role of termination and antitermination. PNAS 105(47):18159–164
doi: 10.1073/pnas.0806084105
Lindahl L (1975) Intermediates and time kinetics of the in vivo assembly of Escherichia coli ribosomes. J Mol Biol 92:15–37
doi: 10.1016/0022-2836(75)90089-3
Michaelis L, Menten M (1913) Die kinetik der invertinwirkung. Biochem Z 49:333–369
Mier-y-Teran-R L, Silber M, Hatzimanakatis V (2010) The origins of time-delay in template bio-polymerization processes. PloS Comput Biol 6(4):1000726
doi: 10.1371/journal.pcbi.1000726
Milo R, Phillips R (2016) Biology by the numbers. Taylor & Francis LLC, New York, Garland Science
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. https://doi.org/10.1038/msb.2009.82
doi: 10.1038/msb.2009.82
Moran U, Phillips R, Milo R (2010) Snapshot: key numbers in biology. Cell 141:1262–1262
doi: 10.1016/j.cell.2010.06.019
Murray HD, Schneider DA, Gourse RL (2003) Control of rRNA expression by small molecules is dynamic and nonredundant. Mol Cell 12(1):125–134. https://doi.org/10.1016/S1097-2765(03)00266-1
doi: 10.1016/S1097-2765(03)00266-1
Paul BJ, Ross W, Gaal T, Gourse RL (2004) rRNA transcription in Escherichia coli. Annu Rev Genet 38(1):749–770. https://doi.org/10.1146/annurev.genet.38.072902.091347 . (PMID: 15568992)
doi: 10.1146/annurev.genet.38.072902.091347
Paul BJ, Barker MM, Ross W, Schneider DA, Webb C, Foster JW, Gourse RL (2004) DksA: a critical component of the transcription initiation machinery that potentiates the regulation of rRNA promoters by ppGpp and the initiating NTP. Cell 118(3):311–322. https://doi.org/10.1016/j.cell.2004.07.009
doi: 10.1016/j.cell.2004.07.009
Reuveni S, Ehrenberg M, Paulsson J (2017) Ribosomes are optimized for autocatalytic production. Nature 547:293–297. https://doi.org/10.1038/nature22998
doi: 10.1038/nature22998
Ross W, Sanchez-Vazquez P, Chen A, Lee J-H, Burgos H, Gourse R (2016) ppGpp binding to a site at the RNAP-DksA interface accounts for its dramatic effects on transcription initiation during the stringent response. Mol Cell 62(6):811–823. https://doi.org/10.1016/j.molcel.2016.04.029
doi: 10.1016/j.molcel.2016.04.029
Ross W, Vrentas C, Sanchez-Vazquez P, Gaal T, Gourse R (2013) The magic spot: a ppGpp binding site on E. coli RNA polymerase responsible for regulation of transcription initiation. Mol Cell 50(3):420–429. https://doi.org/10.1016/j.molcel.2013.03.021
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
doi: 10.1126/science.1192588
Scott M, Klumpp S, Mateescu E, Hwa T (2014) Emergence of robust growth laws from optimal regulation of ribosome synthesis. Mol Syst Biol 10(8):747
doi: 10.15252/msb.20145379
Shaw K (2008) Negative transcription regulation in prokaryotes. Nat Educ 1(1):122
Siwiak M, Zielenkiewicz P (2013) Transimulation - protein biosynthesis web service. PLoS ONE 8(9):73943. https://doi.org/10.1371/journal.pone.0073943
doi: 10.1371/journal.pone.0073943
Srivatsan A, Wang JD (2008) Control of bacterial transcription, translation and replication by (p)ppGpp. Curr Opin Microbiol 11:100–15
doi: 10.1016/j.mib.2008.02.001
Traxler MF, Zacharia VM, Marquardt S, Summers SM, Nguyen H-T, Stark SE, Conway T (2011) Discretely calibrated regulatory loops controlled by ppGpp partition gene induction across the feast to famine gradient in Escherichia coli. Mol Microbiol 79(4):830–845
doi: 10.1111/j.1365-2958.2010.07498.x
Weiße AY, Oyarzún DA, Danos V, Swain PS (2015) Mechanistic links between cellular trade-offs, gene expression, and growth. Proc Natl Acad Sci 112(9):1038–1047. https://doi.org/10.1073/pnas.1416533112
doi: 10.1073/pnas.1416533112
Whitford P, Geggier P, Altman R, Blanchard S, Onuchic J, Sanbonmatsu K (2010) Accommodation of aminoacyl-tRNA into the ribosome involves reversible excursions along multiple pathways. RNA 16:1196–1204
doi: 10.1261/rna.2035410
Yuan J, Fowler W, Kimball E et al (2006) Kinetic flux profiling of nitrogen assimilation in Escherichia coli. Nat Chem Biol 2:529–530
doi: 10.1038/nchembio816
Zampieri M, Hörl M, Hotz F, et al (2019) Regulatory mechanisms underlying coordination of amino acid and glucose catabolism in Escherichia coli. Nat Commun 10(3354). https://doi.org/10.1038/s41467-019-11331-5