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Abstract

Since Jacques Monod's foundational work in the 1940s, investigators studying bacterial physiology have largely (but not exclusively) focused on the exponential phase of bacterial cultures, which is characterized by rapid growth and high biosynthesis activity in the presence of excess nutrients. However, this is not the predominant state of bacterial life. In nature, most bacteria experience nutrient limitation most of the time. In fact, investigators even prior to Monod had identified other aspects of bacterial growth, including what is now known as the stationary phase, when nutrients become limiting. This review will discuss how bacteria transition to growth arrest in response to nutrient limitation through changes in transcription, translation, and metabolism. We will then examine how these changes facilitate survival during potentially extended periods of nutrient limitation, with particular attention to the metabolic strategies that underpin bacterial longevity in this state.

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2022-09-08
2024-05-10
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Literature Cited

  1. 1.
    Aberg A, Fernandez-Vazquez J, Cabrer-Panes JD, Sanchez A, Balsalobre C. 2009. Similar and divergent effects of ppGpp and DksA deficiencies on transcription in Escherichia coli. J. Bacteriol. 191:103226–36
    [Google Scholar]
  2. 2.
    Airas RK. 1996. Differences in the magnesium dependences of the class I and class II aminoacyl-tRNA synthetases from Escherichia coli. Eur. J. Biochem. 240:1223–31
    [Google Scholar]
  3. 3.
    Akanuma G, Kazo Y, Tagami K, Hiraoka H, Yano K et al. 2016. Ribosome dimerization is essential for the efficient regrowth of Bacillus subtilis. Microbiology 162:3448–58
    [Google Scholar]
  4. 4.
    Akiyama T, Williamson KS, Franklin MJ. 2018. Expression and regulation of the Pseudomonas aeruginosa hibernation promoting factor. Mol. Microbiol. 110:2161–75
    [Google Scholar]
  5. 5.
    Akiyama T, Williamson KS, Schaefer R, Pratt S, Chang CB, Franklin MJ. 2017. Resuscitation of Pseudomonas aeruginosa from dormancy requires hibernation promoting factor (PA4463) for ribosome preservation. PNAS 114:123204–9
    [Google Scholar]
  6. 6.
    Alden L, Demoling F, Baath E. 2001. Rapid method of determining factors limiting bacterial growth in soil. Appl. Environ. Microb. 67:41830–38
    [Google Scholar]
  7. 7.
    Amy PS, Morita RY. 1983. Starvation-survival patterns of sixteen freshly isolated open-ocean bacteria. Appl. Environ. Microb. 45:31109–15
    [Google Scholar]
  8. 8.
    Atkinson GC, Tenson T, Hauryliuk V. 2011. The RelA/SpoT homolog (RSH) superfamily: distribution and functional evolution of ppGpp synthetases and hydrolases across the Tree of Life. PLOS ONE 6:8e23479
    [Google Scholar]
  9. 9.
    Aviv M, Giladi H, Oppenheim AB, Glaser G. 1996. Analysis of the shut-off of ribosomal RNA promoters in Escherichia coli upon entering the stationary phase of growth. FEMS Microbiol. Lett. 140:171–76
    [Google Scholar]
  10. 10.
    Babin BM, Bergkessel M, Sweredoski MJ, Moradian A, Hess S et al. 2016. SutA is a bacterial transcription factor expressed during slow growth in Pseudomonas aeruginosa. PNAS 113:5E597–605
    [Google Scholar]
  11. 11.
    Basta DW, Angeles-Albores D, Spero MA, Ciemniecki JA, Newman DK. 2020. Heat-shock proteases promote survival of Pseudomonas aeruginosa during growth arrest. PNAS 117:84358–67
    [Google Scholar]
  12. 12.
    Basta DW, Bergkessel M, Newman DK. 2017. Identification of fitness determinants during energy-limited growth arrest in Pseudomonas aeruginosa. mBio 8:6e01170–17
    [Google Scholar]
  13. 13.
    Basu A, Yap MN. 2016. Ribosome hibernation factor promotes Staphylococcal survival and differentially represses translation. Nucleic Acids Res 44:104881–93
    [Google Scholar]
  14. 14.
    Bergkessel M. 2020. Regulation of protein biosynthetic activity during growth arrest. Curr. Opin. Microbiol. 57:62–69
    [Google Scholar]
  15. 15.
    Bergkessel M, Babin BM, VanderVelde D, Sweredoski MJ, Moradian A et al. 2019. The dormancy-specific regulator, SutA, is intrinsically disordered and modulates transcription initiation in Pseudomonas aeruginosa. Mol. Microbiol. 112:3992–1009
    [Google Scholar]
  16. 16.
    Bergkessel M, Basta DW, Newman DK. 2016. The physiology of growth arrest: uniting molecular and environmental microbiology. Nat. Rev. Microbiol. 14:9549–62
    [Google Scholar]
  17. 17.
    Bergkessel M, Delavaine L. 2021. Diversity in starvation survival strategies and outcomes among heterotrophic proteobacteria. Microb. Physiol. 31:2146–62
    [Google Scholar]
  18. 18.
    Bernhardt J, Weibezahn J, Scharf C, Hecker M. 2003. Bacillus subtilis during feast and famine: visualization of the overall regulation of protein synthesis during glucose starvation by proteome analysis. Genome Res 13:2224–37
    [Google Scholar]
  19. 19.
    Bertrand RL. 2019. Lag phase is a dynamic, organized, adaptive, and evolvable period that prepares bacteria for cell division. J. Bacteriol. 201:7e00697–18
    [Google Scholar]
  20. 20.
    Bigger JW. 1944. Treatment of staphylococcal infections with penicillin by intermittent sterilisation. Lancet 244:497–500
    [Google Scholar]
  21. 21.
    Biselli E, Schink SJ, Gerland U. 2020. Slower growth of Escherichia coli leads to longer survival in carbon starvation due to a decrease in the maintenance rate. Mol. Syst. Biol. 16:6e9478
    [Google Scholar]
  22. 22.
    Boutte CC, Crosson S. 2011. The complex logic of stringent response regulation in Caulobacter crescentus: starvation signalling in an oligotrophic environment. Mol. Microbiol. 80:3695–714
    [Google Scholar]
  23. 23.
    Boutte CC, Henry JT, Crosson S. 2012. ppGpp and polyphosphate modulate cell cycle progression in Caulobacter crescentus. J. Bacteriol. 194:128–35
    [Google Scholar]
  24. 24.
    Brinsmade SR, Alexander EL, Livny J, Stettner AI, Segre D et al. 2014. Hierarchical expression of genes controlled by the Bacillus subtilis global regulatory protein CodY. PNAS 111:228227–32
    [Google Scholar]
  25. 25.
    Brown DR, Barton G, Pan Z, Buck M, Wigneshweraraj S. 2014. Nitrogen stress response and stringent response are coupled in Escherichia coli. Nat. Commun. 5:14115
    [Google Scholar]
  26. 26.
    Buckstein MH, He J, Rubin H. 2008. Characterization of nucleotide pools as a function of physiological state in Escherichia coli. J. Bacteriol. 190:2718–26
    [Google Scholar]
  27. 27.
    Chang DE, Smalley DJ, Tucker DL, Leatham MP, Norris WE et al. 2004. Carbon nutrition of Escherichia coli in the mouse intestine. PNAS 101:197427–32
    [Google Scholar]
  28. 28.
    Church MJ, Hutchins DA, Ducklow HW. 2000. Limitation of bacterial growth by dissolved organic matter and iron in the Southern Ocean. Appl. Environ. Microb. 66:2455–66
    [Google Scholar]
  29. 29.
    Dai X, Zhu M, Warren M, Balakrishnan R, Patsalo V et al. 2016. Reduction of translating ribosomes enables Escherichia coli to maintain elongation rates during slow growth. Nat. Microbiol. 2:216231
    [Google Scholar]
  30. 30.
    Dalebroux ZD, Swanson MS. 2012. ppGpp: magic beyond RNA polymerase. Nat. Rev. Microbiol. 10:3203
    [Google Scholar]
  31. 31.
    Davis BD. 1948. Isolation of biochemically deficient mutants of bacteria by penicillin. J. Am. Chem. Soc. 70:4267
    [Google Scholar]
  32. 32.
    Dawes IW, Mandelstam J. 1970. Sporulation of Bacillus subtilis in continuous culture. J. Bacteriol. 103:3529–35
    [Google Scholar]
  33. 33.
    de Dios R, Santero E, Reyes-Ramírez F. 2021. Extracytoplasmic function σ factors as tools for coordinating stress responses. Int. J. Mol. Sci. 22:83900
    [Google Scholar]
  34. 34.
    Deutscher MP. 2003. Degradation of stable RNA in bacteria. J. Biol. Chem. 278:4645041–44
    [Google Scholar]
  35. 35.
    Diez S, Ryu J, Caban K, Gonzalez RL Jr., Dworkin J. 2020. The alarmones (p)ppGpp directly regulate translation initiation during entry into quiescence. PNAS 117:2715565–72
    [Google Scholar]
  36. 36.
    Dutta NK, Klinkenberg LG, Vazquez M-J, Segura-Carro D, Colmenarejo G et al. 2019. Inhibiting the stringent response blocks Mycobacterium tuberculosis entry into quiescence and reduces persistence. Sci. Adv. 5:3eaav2104
    [Google Scholar]
  37. 37.
    Dworkin J, Shah I. 2010. Exit from dormancy in microbial organisms. Nat. Rev. Microbiol. 8:12890–96
    [Google Scholar]
  38. 38.
    Eschbach M, Schreiber K, Trunk K, Buer J, Jahn D, Schobert M. 2004. Long-term anaerobic survival of the opportunistic pathogen Pseudomonas aeruginosa via pyruvate fermentation. J. Bacteriol. 186:144596–604
    [Google Scholar]
  39. 39.
    Fang M, Bauer CE. 2018. Regulation of stringent factor by branched-chain amino acids. PNAS 115:256446–51
    [Google Scholar]
  40. 40.
    Feaga HA, Dworkin J. 2021. Transcription regulates ribosome hibernation. Mol. Microbiol. 116:2663–73
    [Google Scholar]
  41. 41.
    Feaga HA, Kopylov M, Kim JK, Jovanovic M, Dworkin J. 2020. Ribosome dimerization protects the small subunit. J. Bacteriol. 202:10e00009–20
    [Google Scholar]
  42. 42.
    Fessler M, Gummesson B, Charbon G, Svenningsen SL, Sorensen MA. 2020. Short-term kinetics of rRNA degradation in Escherichia coli upon starvation for carbon, amino acid or phosphate. Mol. Microbiol. 113:5951–63
    [Google Scholar]
  43. 43.
    Finkel SE. 2006. Long-term survival during stationary phase: evolution and the GASP phenotype. Nat. Rev. Microbiol. 4:2113–20
    [Google Scholar]
  44. 44.
    Flardh K, Cohen PS, Kjelleberg S. 1992. Ribosomes exist in large excess over the apparent demand for protein synthesis during carbon starvation in marine Vibrio sp. strain CCUG 15956. J. Bacteriol. 174:216780–88
    [Google Scholar]
  45. 45.
    Gaal T, Bartlett MS, Ross W, Turnbough CL Jr., Gourse RL. 1997. Transcription regulation by initiating NTP concentration: rRNA synthesis in bacteria. Science 278:53462092–97
    [Google Scholar]
  46. 46.
    Gefen O, Fridman O, Ronin I, Balaban NQ. 2014. Direct observation of single stationary-phase bacteria reveals a surprisingly long period of constant protein production activity. PNAS 111:1556–61
    [Google Scholar]
  47. 47.
    Germain E, Guiraud P, Byrne D, Douzi B, Djendli M, Maisonneuve E. 2019. YtfK activates the stringent response by triggering the alarmone synthetase SpoT in Escherichia coli. Nat. Commun. 10:15763
    [Google Scholar]
  48. 48.
    Ghosal A, Babu VMP, Walker GC. 2018. Elevated levels of Era GTPase improve growth, 16S rRNA processing, and 70S ribosome assembly of Escherichia coli lacking highly conserved multifunctional YbeY endoribonuclease. J. Bacteriol. 200:17e00278–18
    [Google Scholar]
  49. 49.
    Gómez-Consarnau L, Akram N, Lindell K, Pedersen A, Neutze R et al. 2010. Proteorhodopsin phototrophy promotes survival of marine bacteria during starvation. PLOS Biol 8:4e1000358
    [Google Scholar]
  50. 50.
    Gonzalez D, Collier J. 2014. Effects of (p)ppGpp on the progression of the cell cycle of Caulobacter crescentus. J. Bacteriol. 196:142514–25
    [Google Scholar]
  51. 51.
    Gosse JL, Engel BJ, Hui JC-H, Harwood CS, Flickinger MC. 2010. Progress toward a biomimetic leaf: 4,000 h of hydrogen production by coating-stabilized nongrowing photosynthetic Rhodopseudomonas palustris. Biotechnol. Progr. 26:4907–18
    [Google Scholar]
  52. 52.
    Gottesman S. 2019. Trouble is coming: signaling pathways that regulate general stress responses in bacteria. J. Biol. Chem. 294:3111685–700
    [Google Scholar]
  53. 53.
    Gourse RL, Chen AY, Gopalkrishnan S, Sanchez-Vazquez P, Myers A, Ross W. 2018. Transcriptional responses to ppGpp and DksA. Annu. Rev. Microbiol. 72:163–84
    [Google Scholar]
  54. 54.
    Green J, Stapleton MR, Smith LJ, Artymiuk PJ, Kahramanoglou C et al. 2014. Cyclic-AMP and bacterial cyclic-AMP receptor proteins revisited: adaptation for different ecological niches. Curr. Opin. Microbiol. 18:1001–7
    [Google Scholar]
  55. 55.
    Groat RG, Schultz JE, Zychlinsky E, Bockman A, Matin A. 1986. Starvation proteins in Escherichia coli: kinetics of synthesis and role in starvation survival. J. Bacteriol. 168:2486–93
    [Google Scholar]
  56. 56.
    Hengge R. 2011. Stationary-phase gene regulation in Escherichia coli section sign. EcoSal Plus. 4:2 https://doi.org/10.1128/ecosalplus.5.6.3
    [Crossref] [Google Scholar]
  57. 57.
    Higgins D, Dworkin J. 2012. Recent progress in Bacillus subtilis sporulation. FEMS Microbiol Rev 36:1131–48
    [Google Scholar]
  58. 58.
    Hoehler TM, Jorgensen BB. 2013. Microbial life under extreme energy limitation. Nat. Rev. Microbiol. 11:283–94
    [Google Scholar]
  59. 59.
    Hood MA, Guckert JB, White DC, Deck F. 1986. Effect of nutrient deprivation on lipid, carbohydrate, DNA, RNA, and protein levels in Vibrio cholerae. Appl. Environ. Microb. 52:4788–93
    [Google Scholar]
  60. 60.
    Imholz NCE, Noga MJ, van den Broek NJF, Bokinsky G. 2020. Calibrating the bacterial growth rate speedometer: a re-evaluation of the relationship between basal ppGpp, growth, and RNA synthesis in Escherichia coli. Front. Microbiol. 11:574872
    [Google Scholar]
  61. 61.
    Irving SE, Choudhury NR, Corrigan RM. 2021. The stringent response and physiological roles of (pp)pGpp in bacteria. Nat. Rev. Microbiol. 19:256–71
    [Google Scholar]
  62. 62.
    James BW, Mauchline WS, Dennis PJ, Keevil CW, Wait R 1999. Poly-3-hydroxybutyrate in Legionella pneumophila, an energy source for survival in low-nutrient environments. Appl. Environ. Microb. 65:2822–27
    [Google Scholar]
  63. 63.
    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. 191:31083–91
    [Google Scholar]
  64. 64.
    Johnson ET, Baron DB, Naranjo B, Bond DR, Schmidt-Dannert C, Gralnick JA. 2010. Enhancement of survival and electricity production in an engineered bacterium by light-driven proton pumping. Appl. Environ. Microb. 76:134123–29
    [Google Scholar]
  65. 65.
    Jubair M, Morris JG, Ali A 2012. Survival of Vibrio cholerae in nutrient-poor environments is associated with a novel “persister” phenotype. PLOS ONE 7:9e45187
    [Google Scholar]
  66. 66.
    Koch AL. 1971. The adaptive responses of Escherichia coli to a feast and famine existence. Adv. Microb. Physiol. 6:147–217
    [Google Scholar]
  67. 67.
    Kolter R, Siegele DA, Tormo A. 1993. The stationary phase of the bacterial life cycle. Annu. Rev. Microbiol. 47:855–74
    [Google Scholar]
  68. 68.
    Kram KE, Henderson AL, Finkel SE. 2020. Escherichia coli has a unique transcriptional program in long-term stationary phase allowing identification of genes important for survival. mSystems 5:4e00364–20
    [Google Scholar]
  69. 69.
    Kriel A, Brinsmade SR, Tse JL, Tehranchi AK, Bittner AN et al. 2014. GTP dysregulation in Bacillus subtilis cells lacking (p)ppGpp results in phenotypic amino acid auxotrophy and failure to adapt to nutrient downshift and regulate biosynthesis genes. J. Bacteriol. 196:1189–201
    [Google Scholar]
  70. 70.
    Lazzarini RA, Cashel M, Gallant J 1971. On the regulation of guanosine tetraphosphate levels in stringent and relaxed strains of Escherichia coli. J. Biol. Chem. 246:438185
    [Google Scholar]
  71. 71.
    Lederberg J, Zinder N. 1948. Concentration of biochemical mutants of bacteria with penicillin. J. Am. Chem. Soc. 70:4267
    [Google Scholar]
  72. 72.
    Lee JW, Park YH, Seok YJ. 2018. Rsd balances (p)ppGpp level by stimulating the hydrolase activity of SpoT during carbon source downshift in Escherichia coli. PNAS 115:29E6845–54
    [Google Scholar]
  73. 73.
    Lempp M, Lubrano P, Bange G, Link H. 2020. Metabolism of non-growing bacteria. Biol. Chem. 401:121479–85
    [Google Scholar]
  74. 74.
    Lever MA, Rogers KL, Lloyd KG, Overmann J, Schink B et al. 2015. Life under extreme energy limitation: a synthesis of laboratory- and field-based investigations. FEMS Microbiol Rev 39:5688–728
    [Google Scholar]
  75. 75.
    Lewenza S, Abboud J, Poon K, Kobryn M, Humplik I et al. 2018. Pseudomonas aeruginosa displays a dormancy phenotype during long-term survival in water. PLOS ONE 13:9e0198384
    [Google Scholar]
  76. 76.
    Li GW, Burkhardt D, Gross C, Weissman JS. 2014. Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources. Cell 157:3624–35
    [Google Scholar]
  77. 77.
    Li SH, Li Z, Park JO, King CG, Rabinowitz JD et al. 2018. Escherichia coli translation strategies differ across carbon, nitrogen and phosphorus limitation conditions. Nat. Microbiol. 3:8939–47
    [Google Scholar]
  78. 78.
    Libby EA, Reuveni S, Dworkin J. 2019. Multisite phosphorylation drives phenotypic variation in (p)ppGpp synthetase-dependent antibiotic tolerance. Nat. Commun. 10:15133
    [Google Scholar]
  79. 79.
    Lopez JM, Dromerick A, Freese E. 1981. Response of guanosine 5′-triphosphate concentration to nutritional changes and its significance for Bacillus subtilis sporulation. J. Bacteriol. 146:2605–13
    [Google Scholar]
  80. 80.
    Lopez JM, Marks CL, Freese E. 1979. The decrease of guanine nucleotides initiates sporulation of Bacillus subtilis. Biochim. Biophys. Acta Gen. Subj. 587:2238–52
    [Google Scholar]
  81. 81.
    Lusk JE, Williams RJ, Kennedy EP. 1968. Magnesium and the growth of Escherichia coli. J. Biol. Chem. 243:2618–24
    [Google Scholar]
  82. 82.
    Machreki Y, Kouidhi B, Machreki S, Chaieb K, Sáenz Y. 2019. Analysis of a long term starved Pseudomonas aeruginosa ATCC27853 in seawater microcosms. Microb. Pathogenesis. 134:103595
    [Google Scholar]
  83. 83.
    Magasanik B. 1988. Reversible phosphorylation of an enhancer binding protein regulates the transcription of bacterial nitrogen utilization genes. Trends Biochem. Sci. 13:475–79
    [Google Scholar]
  84. 84.
    Magnusson LU, Farewell A, Nyström T. 2005. ppGpp: a global regulator in Escherichia coli. Trends Microbiol 13:5236–42
    [Google Scholar]
  85. 85.
    Maisonneuve E, Gerdes K. 2014. Molecular mechanisms underlying bacterial persisters. Cell 157:3539–48
    [Google Scholar]
  86. 86.
    Makman RS, Sutherland EW. 1965. Adenosine 3′,5′-phosphate in Escherichia coli. J. Biol. Chem. 240:1309–14
    [Google Scholar]
  87. 87.
    McIntosh M, Eisenhardt K, Remes B, Konzer A, Klug G. 2019. Adaptation of the alphaproteobacterium Rhodobacter sphaeroides to stationary phase. Environ. Microbiol. 21:114425–45
    [Google Scholar]
  88. 88.
    Metzger S, Schreiber G, Aizenman E, Cashel M, Glaser G. 1989. Characterization of the relA1 mutation and a comparison of relA1 with new relA null alleles in Escherichia coli. J. Biol. Chem. 264:21146–52
    [Google Scholar]
  89. 89.
    Monod J. 1949. The growth of bacterial cultures. Annu. Rev. Microbiol. 3:371–94
    [Google Scholar]
  90. 90.
    Moore RA, Tuanyok A, Woods DE. 2008. Survival of Burkholderia pseudomallei in water. BMC Res. Notes 1:111
    [Google Scholar]
  91. 91.
    Murray DK, Bremer H. 1996. Control of spoT-dependent ppGpp synthesis and degradation in Escherichia coli. J. Mol. Biol. 259:141–57
    [Google Scholar]
  92. 92.
    Murray HD, Schneider DA, Gourse RL. 2003. Control of rRNA expression by small molecules is dynamic and nonredundant. Mol. Cell 12:1125–34
    [Google Scholar]
  93. 93.
    Nguyen D, Joshi-Datar A, Lepine F, Bauerle E, Olakanmi O et al. 2011. Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science 334:6058982–86
    [Google Scholar]
  94. 94.
    Notley-McRobb L, Death A, Ferenci T. 1997. The relationship between external glucose concentration and cAMP levels inside Escherichia coli: implications for models of phosphotransferase-mediated regulation of adenylate cyclase. Microbiology 143:Part 61909–18
    [Google Scholar]
  95. 95.
    O'Farrell PH. 1978. The suppression of defective translation by ppGpp and its role in the stringent response. Cell 14:3545–57
    [Google Scholar]
  96. 96.
    Oldewurtel ER, Kitahara Y, van Teeffelen S. 2021. Robust surface-to-mass coupling and turgor-dependent cell width determine bacterial dry-mass density. PNAS 118:32e2021416118
    [Google Scholar]
  97. 97.
    Parker DJ, Lalanne JB, Kimura S, Johnson GE, Waldor MK, Li GW. 2020. Growth-optimized aminoacyl-tRNA synthetase levels prevent maximal tRNA charging. Cell Syst 11:2121–30.e6
    [Google Scholar]
  98. 98.
    Pechter KB, Yin L, Oda Y, Gallagher L, Yang J et al. 2017. Molecular basis of bacterial longevity. mBio 8:6e01726–17
    [Google Scholar]
  99. 99.
    Pereira SF, Gonzalez RL Jr., Dworkin J. 2015. Protein synthesis during cellular quiescence is inhibited by phosphorylation of a translational elongation factor. PNAS 112:25E3274–81
    [Google Scholar]
  100. 100.
    Poindexter JS. 1981. Oligotrophy: fast and famine existence. Adv. Microb. Ecol. 5:63–90
    [Google Scholar]
  101. 101.
    Pontes MH, Groisman EA. 2018. Protein synthesis controls phosphate homeostasis. Gene Dev 32:179–92
    [Google Scholar]
  102. 102.
    Pontes MH, Groisman EA. 2019. Slow growth determines nonheritable antibiotic resistance in Salmonella enterica. Sci. Signal. 12:592eaax3938
    [Google Scholar]
  103. 103.
    Pontes MH, Yeom J, Groisman EA. 2016. Reducing ribosome biosynthesis promotes translation during low Mg2+ stress. Mol. Cell 64:3480–92
    [Google Scholar]
  104. 104.
    Potrykus K, Cashel M. 2008. (p)ppGpp: still magical?. Annu. Rev. Microbiol. 62:35–51
    [Google Scholar]
  105. 105.
    Price MN, Zane GM, Kuehl JV, Melnyk RA, Wall JD et al. 2018. Filling gaps in bacterial amino acid biosynthesis pathways with high-throughput genetics. PLOS Genet 14:1e1007147
    [Google Scholar]
  106. 106.
    Prossliner T, Winther KS, Sorensen MA, Gerdes K. 2018. Ribosome hibernation. Annu. Rev. Genet. 52:32148
    [Google Scholar]
  107. 107.
    Prusa J, Zhu DX, Stallings CL. 2018. The stringent response and Mycobacterium tuberculosis pathogenesis. Pathog. Dis. 76:5fty054
    [Google Scholar]
  108. 108.
    Puszynska AM, O'Shea EK 2017. ppGpp controls global gene expression in light and in darkness in S. elongatus. Cell Rep 21:113155–65
    [Google Scholar]
  109. 109.
    Rao SPS, Alonso S, Rand L, Dick T, Pethe K. 2008. The protonmotive force is required for maintaining ATP homeostasis and viability of hypoxic, nonreplicating Mycobacterium tuberculosis. PNAS 105:3311945–50
    [Google Scholar]
  110. 110.
    Ratnayake-Lecamwasam M, Serror P, Wong KW, Sonenshein AL. 2001. Bacillus subtilis CodY represses early-stationary-phase genes by sensing GTP levels. Gene Dev 15:91093–103
    [Google Scholar]
  111. 111.
    Reeve CA, Amy PS, Matin A. 1984. Role of protein synthesis in the survival of carbon-starved Escherichia coli K-12. J. Bacteriol. 160:31041–46
    [Google Scholar]
  112. 112.
    Remigi P, Ferguson GC, McConnell E, Monte SD, Rogers DW, Rainey PB. 2019. Ribosome provisioning activates a bistable switch coupled to fast exit from stationary phase. Mol. Biol. Evol. 36:51056–70
    [Google Scholar]
  113. 113.
    Riley EP, Lopez-Garrido J, Sugie J, Liu RB, Pogliano K. 2021. Metabolic differentiation and intercellular nurturing underpin bacterial endospore formation. Sci. Adv. 7:4eabd6385
    [Google Scholar]
  114. 114.
    Rittershaus ES, Baek SH, Sassetti CM. 2013. The normalcy of dormancy: common themes in microbial quiescence. Cell Host Microbe 13:6643–51
    [Google Scholar]
  115. 115.
    Russell JB, Cook GM. 1995. Energetics of bacterial growth: balance of anabolic and catabolic reactions. Microbiol. Rev. 59:48–62
    [Google Scholar]
  116. 116.
    Sanchez-Vazquez P, Dewey CN, Kitten N, Ross W, Gourse RL 2019. Genome-wide effects on Escherichia coli transcription from ppGpp binding to its two sites on RNA polymerase. PNAS 116:178310–19
    [Google Scholar]
  117. 117.
    Schaeffer P, Millet J, Aubert JP 1965. Catabolic repression of bacterial sporulation. PNAS 54:3704–11
    [Google Scholar]
  118. 118.
    Schink SJ, Biselli E, Ammar C, Gerland U. 2019. Death rate of Escherichia coli during starvation is set by maintenance cost and biomass recycling. Cell Syst 9:164–73.e3
    [Google Scholar]
  119. 119.
    Schreiber G, Metzger S, Aizenman E, Roza S, Cashel M, Glaser G. 1991. Overexpression of the relA gene in Escherichia coli. J. Biol. Chem. 266:3760–67
    [Google Scholar]
  120. 120.
    Seif Y, Choudhary KS, Hefner Y, Anand A, Yang L, Palsson BO. 2020. Metabolic and genetic basis for auxotrophies in Gram-negative species. PNAS 117:116264–73
    [Google Scholar]
  121. 121.
    Sekar K, Linker SM, Nguyen J, Grünhagen A, Stocker R, Sauer U. 2020. Bacterial glycogen provides short-term benefits in changing environments. Appl. Environ. Microb. 86:9e00049–20
    [Google Scholar]
  122. 122.
    Shi H, Hu Y, Odermatt PD, Gonzalez CG, Zhang L et al. 2021. Precise regulation of the relative rates of surface area and volume synthesis in bacterial cells growing in dynamic environments. Nat. Commun. 12:11975
    [Google Scholar]
  123. 123.
    Shyp V, Dubey BN, Bohm R, Hartl J, Nesper J et al. 2021. Reciprocal growth control by competitive binding of nucleotide second messengers to a metabolic switch in Caulobacter crescentus. Nat. Microbiol. 6:159–72
    [Google Scholar]
  124. 124.
    Sonenshein AL. 2005. CodY, a global regulator of stationary phase and virulence in Gram-positive bacteria. Curr. Opin. Microbiol. 8:2203–7
    [Google Scholar]
  125. 125.
    Song Y, Cartron ML, Jackson PJ, Davison PA, Dickman MJ et al. 2019. Proteorhodopsin overproduction enhances the long-term viability of Escherichia coli. Appl. Environ. Microb. 86:1e02087–19
    [Google Scholar]
  126. 126.
    Spira B, Silberstein N, Yagil E. 1995. Guanosine 3′,5′-bispyrophosphate (ppGpp) synthesis in cells of Escherichia coli starved for Pi. J. Bacteriol. 177:144053–58
    [Google Scholar]
  127. 127.
    Srivatsan A, Wang JD. 2008. Control of bacterial transcription, translation and replication by (p)ppGpp. Curr. Opin. Microbiol. 11:2100–5
    [Google Scholar]
  128. 128.
    Starosta AL, Lassak J, Jung K, Wilson DN 2014. The bacterial translation stress response. FEMS Microbiol. Rev. 38:61172–201
    [Google Scholar]
  129. 129.
    Stouthamer AH. 1973. A theoretical study on the amount of ATP required for synthesis of microbial cell material. Antonie Van Leeuwenhoek 39:1545–65
    [Google Scholar]
  130. 130.
    Strange RE. 1968. Bacterial “glycogen” and survival. Nature 220:5167606–7
    [Google Scholar]
  131. 131.
    Switzer A, Burchell L, McQuail J, Wigneshweraraj S. 2020. The adaptive response to long-term nitrogen starvation in Escherichia coli requires the breakdown of allantoin. J. Bacteriol. 202:17e00172–20
    [Google Scholar]
  132. 132.
    Takano S, Pawlowska BJ, Gudelj I, Yomo T, Tsuru S. 2017. Density-dependent recycling promotes the long-term survival of bacterial populations during periods of starvation. mBio 8:1e02336–16
    [Google Scholar]
  133. 133.
    Tomar SK, Kumar P, Prakash B. 2011. Deciphering the catalytic machinery in a universally conserved ribosome binding ATPase YchF. Biochem. Biophys. Res. Commun. 408:3459–64
    [Google Scholar]
  134. 134.
    Varik V, Oliveira SRA, Hauryliuk V, Tenson T. 2017. HPLC-based quantification of bacterial housekeeping nucleotides and alarmone messengers ppGpp and pppGpp. Sci. Rep. 7:111022
    [Google Scholar]
  135. 135.
    Vercruysse M, Köhrer C, Shen Y, Proulx S, Ghosal A et al. 2016. Identification of YbeY-protein interactions involved in 16S rRNA maturation and stress regulation in Escherichia coli. mBio 7:6e01785–16
    [Google Scholar]
  136. 136.
    Villadsen IS, Michelsen O. 1977. Regulation of PRPP and nucleoside tri and tetraphosphate pools in Escherichia coli under conditions of nitrogen starvation. J. Bacteriol. 130:1136–43
    [Google Scholar]
  137. 137.
    Villapakkam AC, Handke LD, Belitsky BR, Levdikov VM, Wilkinson AJ, Sonenshein AL. 2009. Genetic and biochemical analysis of the interaction of Bacillus subtilis CodY with branched-chain amino acids. J. Bacteriol. 191:226865–76
    [Google Scholar]
  138. 138.
    Wang B, Dai P, Ding D, Del Rosario A, Grant RA et al. 2019. Affinity-based capture and identification of protein effectors of the growth regulator ppGpp. Nat. Chem. Biol. 15:14150
    [Google Scholar]
  139. 139.
    Wood A, Irving SE, Bennison DJ, Corrigan RM. 2019. The (p)ppGpp-binding GTPase Era promotes rRNA processing and cold adaptation in Staphylococcus aureus. PLOS Genet. 15:8e1008346
    [Google Scholar]
  140. 140.
    Yang J, Yin L, Lessner FH, Nakayasu ES, Payne SH et al. 2017. Genes essential for phototrophic growth by a purple alphaproteobacterium. Environ. Microbiol. 19:93567–78
    [Google Scholar]
  141. 141.
    Yin L, Harwood CS. 2019. Functional divergence of annotated l-isoaspartate O-methyltransferases in an α-proteobacterium. J. Biol. Chem. 294:82854–61
    [Google Scholar]
  142. 142.
    Yin L, Ma H, Nakayasu ES, Payne SH, Morris DR, Harwood CS. 2019. Bacterial longevity requires protein synthesis and a stringent response. mBio 10:5e02189–19
    [Google Scholar]
  143. 143.
    Zambrano MM, Siegele DA, Almirón M, Tormo A, Kolter R. 1993. Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science 259:51021757–60
    [Google Scholar]
  144. 144.
    Zgurskaya HI, Keyhan M, Matin A. 1997. The σS level in starving Escherichia coli cells increases solely as a result of its increased stability, despite decreased synthesis. Mol. Microbiol. 24:3643–51
    [Google Scholar]
  145. 145.
    Zhang Y, Zborníková E, Rejman D, Gerdes K. 2018. Novel (p)ppGpp binding and metabolizing proteins of Escherichia coli. mBio 9:2e02188–17
    [Google Scholar]
  146. 146.
    Zinser ER, Kolter R. 2004. Escherichia coli evolution during stationary phase. Res. Microbiol. 155:5328–36
    [Google Scholar]
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