1932

Abstract

Temperature impacts biological systems across all length and timescales. Cells and the enzymes that comprise them respond to temperature fluctuations on short timescales, and temperature can affect protein folding, the molecular composition of cells, and volume expansion. Entire ecosystems exhibit temperature-dependent behaviors, and global warming threatens to disrupt thermal homeostasis in microbes that are important for human and planetary health. Intriguingly, the growth rate of most species follows the Arrhenius law of equilibrium thermodynamics, with an activation energy similar to that of individual enzymes but with maximal growth rates and over temperature ranges that are species specific. In this review, we discuss how the temperature dependence of critical cellular processes, such as the central dogma and membrane fluidity, contributes to the temperature dependence of growth. We conclude with a discussion of adaptation to temperature shifts and the effects of temperature on evolution and on the properties of microbial ecosystems.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-112221-074832
2022-05-09
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/biophys/51/1/annurev-biophys-112221-074832.html?itemId=/content/journals/10.1146/annurev-biophys-112221-074832&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Abbondanzieri EA, Shaevitz JW, Block SM. 2005. Picocalorimetry of transcription by RNA polymerase. Biophys. J. 89:6L61–63
    [Google Scholar]
  2. 2.
    Al Refaii A, Alix JH 2009. Ribosome biogenesis is temperature-dependent and delayed in Escherichia coli lacking the chaperones DnaK or DnaJ. Mol. Microbiol. 71:3748–62
    [Google Scholar]
  3. 3.
    Al Saleh AA. 1983. Effects of temperature on the replication of chromosomal DNA of Xenopus laevis cells. J. Cell Sci. 59:1–12
    [Google Scholar]
  4. 4.
    Almeida PFF, Vaz WLC, Thompson TE. 1992. Lateral diffusion in the liquid phases of dimyristoylphosphatidylcholine/cholesterol lipid bilayers: a free volume analysis. Biochemistry 31:296739–47
    [Google Scholar]
  5. 5.
    Anderson RL, Minton KW, Li GC, Hahn GM 1981. Temperature-induced homeoviscous adaptation of Chinese hamster ovary cells. Biochim. Biophys. Acta Biomembr. 641:2334–48
    [Google Scholar]
  6. 6.
    Araki T. 1991. The effect of temperature shifts on protein synthesis by the psychrophilic bacterium Vibrio sp. strain ANT-300. J. Gen. Microbiol. 137:4817–26
    [Google Scholar]
  7. 6a.
    Aranda-Díaz A, Ng KM, Thomsen T, Real-Ramírez I, Dahan Det al 2022. Establishment and characterization of stable, diverse, fecal-derived in vitro microbial communities that model the intestinal microbiota. Cell Host Microbe 30:226072.e5
    [Google Scholar]
  8. 7.
    Arcus VL, Mulholland AJ. 2020. Temperature, dynamics, and enzyme-catalyzed reaction rates. Annu. Rev. Biophys. 49:163–80
    [Google Scholar]
  9. 8.
    Arrhenius S. 1889. Über die Reaktionsgeschwindigkeit bei der Inversion von Rohrzucker durch Säuren. Z. Phys. Chem. 4U:1226–48
    [Google Scholar]
  10. 9.
    Balleza E, Kim JM, Cluzel P. 2018. Systematic characterization of maturation time of fluorescent proteins in living cells. Nat. Methods 15:147–51
    [Google Scholar]
  11. 10.
    Barber MA. 1908. The rate of multiplication of Bacillus coli at different temperatures. J. Infect. Dis. 5:4379–400
    [Google Scholar]
  12. 11.
    Bárcenas-Moreno G, Brandón MG, Rousk J, Bååth E 2009. Adaptation of soil microbial communities to temperature: comparison of fungi and bacteria in a laboratory experiment. Glob. Change Biol. 15:122950–57
    [Google Scholar]
  13. 12.
    Bennett AF, Lenski RE, Mittler JE. 1992. Evolutionary adaptation to temperature. I. Fitness responses of Escherichia coli to changes in its thermal environment. Evolution 46:116–30
    [Google Scholar]
  14. 13.
    Brown HS, Licata VJ. 2013. Enthalpic switch-points and temperature dependencies of DNA binding and nucleotide incorporation by Pol I DNA polymerases. Biochim. Biophys. Acta Proteins Proteom. 1834:102133–38
    [Google Scholar]
  15. 14.
    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]
  16. 15.
    Budin I, de Rond T, Chen Y, Chan LJG, Petzold CJ, Keasling JD. 2018. Viscous control of cellular respiration by membrane lipid composition. Science 362:64191186–89
    [Google Scholar]
  17. 16.
    Çaglayan M, Bilgin N. 2012. Temperature dependence of accuracy of DNA polymerase I from Geobacillus anatolicus. Biochimie 94:91968–73
    [Google Scholar]
  18. 17.
    Casadevall A. 2012. Fungi and the rise of mammals. PLOS Pathog 8:8e1002808
    [Google Scholar]
  19. 18.
    Cavicchioli R, Ripple WJ, Timmis KN, Azam F, Bakken LR et al. 2019. Scientists’ warning to humanity: microorganisms and climate change. Nat. Rev. Microbiol. 17:9569–86
    [Google Scholar]
  20. 19.
    Chapman JD, Pollard EC. 1969. Characteristics of the enzymatic breakdown of DNA in Escherichia coli in response to ionizing radiation. Int. J. Radiat. Biol. 15:4323–33
    [Google Scholar]
  21. 20.
    Chen K, Gao Y, Mih N, O'Brien EJ, Yang L, Palsson BO 2017. Thermosensitivity of growth is determined by chaperone-mediated proteome reallocation. PNAS 114:4311548–53
    [Google Scholar]
  22. 21.
    Chohji T, Sawada T, Kuno S. 1976. Macromolecule synthesis in Escherichia coli BB under various growth conditions. Appl. Environ. Microbiol. 31:6864–69
    [Google Scholar]
  23. 22.
    Chrétien D, Bénit P, Ha HH, Keipert S, El-Khoury R et al. 2018. Mitochondria are physiologically maintained at close to 50°C. PLOS Biol 16:1e2003992
    [Google Scholar]
  24. 23.
    Corkrey R, McMeekin TA, Bowman JP, Ratkowsky DA, Olley J, Ross T 2016. The biokinetic spectrum for temperature. PLOS ONE 11:4e0153343
    [Google Scholar]
  25. 24.
    Corkrey R, Olley J, Ratkowsky D, McMeekin T, Ross T 2012. Universality of thermodynamic constants governing biological growth rates. PLOS ONE 7:2e32003
    [Google Scholar]
  26. 25.
    Cossins AR, Prosser CL. 1978. Evolutionary adaptation of membranes to temperature. PNAS 75:42040–43
    [Google Scholar]
  27. 26.
    Crick FHC. 1966. Codon–anticodon pairing: the wobble hypothesis. J. Mol. Biol. 19:2548–55
    [Google Scholar]
  28. 27.
    Darland G, Brock TD. 1971. Bacillus acidocaldarius sp. nov., an acidophilic thermophilic spore-forming bacterium. J. Gen. Microbiol. 67:19–15
    [Google Scholar]
  29. 28.
    Datta K, LiCata VJ. 2003. Thermodynamics of the binding of Thermus aquaticus DNA polymerase to primed-template DNA. Nucleic Acids Res 31:195590–97
    [Google Scholar]
  30. 29.
    Datta K, Wowor AJ, Richard AJ, Licata VJ 2006. Temperature dependence and thermodynamics of Klenow polymerase binding to primed-template DNA. Biophys. J. 90:51739–51
    [Google Scholar]
  31. 30.
    DeAngelis KM, Pold G, Topçuoglu BD, van Diepen LTA, Varney RM et al. 2015. Long-term forest soil warming alters microbial communities in temperate forest soils. Front. Microbiol. 6:104
    [Google Scholar]
  32. 31.
    Deatherage DE, Kepner JL, Bennett AF, Lenski RE, Barrick JE. 2017. Specificity of genome evolution in experimental populations of Escherichia coli evolved at different temperatures. PNAS 114:10E1904–12
    [Google Scholar]
  33. 32.
    Debey P, Hoa GHB, Douzou P, Godefroy-Colburn T, Graffe M, Grunberg-Manago M. 1975. Ribosomal subunit interaction as studied by light scattering: evidence of different classes of ribosome preparations. Biochemistry 14:81553–59
    [Google Scholar]
  34. 33.
    Dill KA, Ghosh K, Schmit JD. 2011. Physical limits of cells and proteomes. PNAS 108:4417876–82
    [Google Scholar]
  35. 34.
    Dong H, Nilsson L, Kurland CG. 1996. Co-variation of tRNA abundance and codon usage in Escherichia coli at different growth rates. J. Mol. Biol. 260:5649–63
    [Google Scholar]
  36. 35.
    Driessen RPC, Sitters G, Laurens N, Moolenaar GF, Wuite GJL et al. 2014. Effect of temperature on the intrinsic flexibility of DNA and its interaction with architectural proteins. Biochemistry 53:416430–38
    [Google Scholar]
  37. 36.
    Duval-Valentin G, Ehrlich R 1987. Dynamic and structural characterisation of multiple steps during complex formation between E. coli RNA polymerase and the tetR promoter from pSC101. Nucleic Acids Res 15:2575–94
    [Google Scholar]
  38. 37.
    Elias M, Wieczorek G, Rosenne S, Tawfik DS 2014. The universality of enzymatic rate-temperature dependency. Trends Biochem. Sci. 39:11–7
    [Google Scholar]
  39. 38.
    Enquist BJ, Economo EP, Huxman TE, Allen AP, Ignace DD, Gillooly JF 2003. Scaling metabolism from organisms to ecosystems. Nature 423:6940639–42
    [Google Scholar]
  40. 39.
    Eyring H. 1935. The activated complex in chemical reactions. J. Chem. Phys. 3:263–71
    [Google Scholar]
  41. 40.
    Farewell A, Neidhardt FC. 1998. Effect of temperature on in vivo protein synthetic capacity in Escherichia coli. J. Bacteriol. 180:174704–10
    [Google Scholar]
  42. 41.
    Fehling E, Weidner M. 1986. Temperature characteristics and adaptive potential of wheat ribosomes. Plant Physiol 80:1181–86
    [Google Scholar]
  43. 42.
    Fiala KA, Sherrer SM, Brown JA, Suo Z. 2008. Mechanistic consequences of temperature on DNA polymerization catalyzed by a Y-family DNA polymerase. Nucleic Acids Res 36:61990–2001
    [Google Scholar]
  44. 43.
    Fiil NP, von Meyenburg K, Friesen JD. 1972. Accumulation and turnover of guanosine tetraphosphate in Escherichia coli. J. Mol. Biol. 71:3769–83
    [Google Scholar]
  45. 44.
    Fijalkowska IJ, Schaaper RM, Jonczyk P. 2012. DNA replication fidelity in Escherichia coli: a multi-DNA polymerase affair. FEMS Microbiol. Rev. 36:61105–21
    [Google Scholar]
  46. 45.
    Frey SD, Drijber R, Smith H, Melillo J 2008. Microbial biomass, functional capacity, and community structure after 12 years of soil warming. Soil Biol. Biochem. 40:112904–7
    [Google Scholar]
  47. 46.
    Frieler K, Meinshausen M, Golly A, Mengel M, Lebek K et al. 2013. Limiting global warming to 2°C is unlikely to save most coral reefs. Nat. Clim. Change 3:2165–70
    [Google Scholar]
  48. 47.
    Gadgil M, Kapur V, Hu WS. 2005. Transcriptional response of Escherichia coli to temperature shift. Biotechnol. Prog. 21:3689–99
    [Google Scholar]
  49. 48.
    Galtier N, Lobry JR. 1997. Relationships between genomic G+C content, RNA secondary structures, and optimal growth temperature in prokaryotes. J. Mol. Evol. 44:6632–36
    [Google Scholar]
  50. 49.
    Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL. 2001. Effects of size and temperature on metabolic rate. Science 293:55382248–51
    [Google Scholar]
  51. 50.
    Goldford JE, Lu N, Bajić D, Estrela S, Tikhonov M et al. 2018. Emergent simplicity in microbial community assembly. Science 361:6401469–74
    [Google Scholar]
  52. 51.
    Gould BS, Sizer IW. 1938. The mechanism of bacterial dehydrogenase activity in vivo. J. Biol. Chem. 124:1269–79
    [Google Scholar]
  53. 52.
    Gruener N, Avi-Dor Y. 1966. Temperature-dependence of activation and inhibition of rat-brain adenosine triphosphatase activated by sodium and potassium ions. Biochem. J. 100:3762–67
    [Google Scholar]
  54. 53.
    Hassan N, Anesio AM, Rafiq M, Holtvoeth J, Bull I et al. 2020. Temperature driven membrane lipid adaptation in glacial psychrophilic bacteria. Front. Microbiol. 11:824
    [Google Scholar]
  55. 54.
    Herendeen SL, VanBogelen RA, Neidhardt FC. 1979. Levels of major proteins of Escherichia coli during growth at different temperatures. J. Bacteriol. 139:1185–94
    [Google Scholar]
  56. 55.
    Herrero AA, Gomez RF. 1980. Development of ethanol tolerance in Clostridium thermocellum: effect of growth temperature. Appl. Environ. Microbiol. 40:3571–77
    [Google Scholar]
  57. 56.
    Hinshelwood SCN. 1952. On the chemical kinetics of autosynthetic systems. J. Chem. Soc. 1952:745–55
    [Google Scholar]
  58. 57.
    Hoa GHB, Graffe M, Grunberg-Manago M. 1977. Thermodynamic studies of the reversible association of Escherichia coli ribosomal subunits. Biochemistry 16:122800–5
    [Google Scholar]
  59. 58.
    Hurst LD, Merchant AR. 2001. High guanine-cytosine content is not an adaptation to high temperature: a comparative analysis amongst prokaryotes. Proc. R. Soc. B 268:1466493–97
    [Google Scholar]
  60. 59.
    Hutchins DA, Jansson JK, Remais JV, Rich VI, Singh BK, Trivedi P. 2019. Climate change microbiology—problems and perspectives. Nat. Rev. Microbiol. 17:6391–96
    [Google Scholar]
  61. 60.
    Iyer-Biswas S, Wright CS, Henry JT, Lo K, Burov S et al. 2014. Scaling laws governing stochastic growth and division of single bacterial cells. PNAS 111:4515912–17
    [Google Scholar]
  62. 61.
    Jansson JK, Hofmockel KS. 2020. Soil microbiomes and climate change. Nat. Rev. Microbiol. 18:135–46
    [Google Scholar]
  63. 62.
    Johansson M, Bouakaz E, Lovmar M, Ehrenberg M 2008. The kinetics of ribosomal peptidyl transfer revisited. Mol. Cell 30:5589–98
    [Google Scholar]
  64. 63.
    Johnson RS, Chester RE 1998. Stopped-flow kinetic analysis of the interaction of Escherichia coli RNA polymerase with the bacteriophage T7 A1 promoter. J. Mol. Biol. 283:2353–70
    [Google Scholar]
  65. 64.
    Jurburg SD, Nunes I, Brejnrod A, Jacquiod S, Priemé A et al. 2017. Legacy effects on the recovery of soil bacterial communities from extreme temperature perturbation. Front. Microbiol. 8:1832
    [Google Scholar]
  66. 65.
    Katunin VI, Savelsbergh A, Rodnina MV, Wintermeyer W. 2002. Coupling of GTP hydrolysis by elongation factor G to translocation and factor recycling on the ribosome. Biochemistry 41:4212806–12
    [Google Scholar]
  67. 66.
    Kawashima T, Amano N, Koike H, Makino SI, Higuchi S et al. 2000. Archaeal adaptation to higher temperatures revealed by genomic sequence of Thermoplasma volcanium. PNAS 97:2614257–62
    [Google Scholar]
  68. 67.
    Knapp BD, Zhu L, Huang KC. 2020. SiCTeC: an inexpensive, easily assembled Peltier device for rapid temperature shifting during single-cell imaging. PLOS Biol 18:11e3000786
    [Google Scholar]
  69. 68.
    Köhler JR, Hube B, Puccia R, Casadevall A, Perfect JR. 2017. Fungi that infect humans. Microbiol. Spectr. 5:3 https://doi.org/10.1128/microbiolspec.FUNK-0014-2016
    [Crossref] [Google Scholar]
  70. 69.
    Kong H, Kucera RB, Jack WE. 1993. Characterization of a DNA polymerase from the hyperthermophile archaea Thermococcus litoralis: vent DNA polymerase, steady state kinetics, thermal stability, processivity, strand displacement, and exonuclease activities. J. Biol. Chem. 268:31965–75
    [Google Scholar]
  71. 70.
    Kortmann J, Narberhaus F. 2012. Bacterial RNA thermometers: molecular zippers and switches. Nat. Rev. Microbiol. 10:4255–65
    [Google Scholar]
  72. 71.
    Kowalak JA, Dalluge JJ, McCloskey JA, Stetter KO. 1994. The role of posttranscriptional modification in stabilization of transfer RNA from hyperthermophiles. Biochemistry 33:257869–76
    [Google Scholar]
  73. 72.
    Kuhlenkoetter S, Wintermeyer W, Rodnina M V. 2011. Different substrate-dependent transition states in the active site of the ribosome. Nature 476:7360351–54
    [Google Scholar]
  74. 73.
    Langer A, Schräml M, Strasser R, Daub H, Myers T et al. 2015. Polymerase/DNA interactions and enzymatic activity: multi-parameter analysis with electro-switchable biosurfaces. Sci. Rep. 5:12066
    [Google Scholar]
  75. 74.
    LaRiviere FJ, Wolfson AD, Uhlenbeck OC. 2001. Uniform binding of aminoacyl-tRNAs to elongation factor Tu by thermodynamic compensation. Science 294:5540165–68
    [Google Scholar]
  76. 75.
    Lax S, Abreu CI, Gore J. 2020. Higher temperatures generically favour slower-growing bacterial species in multispecies communities. Nat. Ecol. Evol. 4:4560–67
    [Google Scholar]
  77. 76.
    Lemaux PG, Herendeen SL, Bloch PL, Neidhardt FC. 1978. Transient rates of synthesis of individual polypeptides in E. coli following temperature shifts. Cell 13:3427–34
    [Google Scholar]
  78. 77.
    Leung EKY, Suslov N, Tuttle N, Sengupta R, Piccirilli JA. 2011. The mechanism of peptidyl transfer catalysis by the ribosome. Annu. Rev. Biochem. 80:527–55
    [Google Scholar]
  79. 78.
    Li G-W, Burkhardt D, Gross C, Weissman JS, Babu M et al. 2014. Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources. Cell 157:3624–35
    [Google Scholar]
  80. 79.
    Lindahl L. 1975. Intermediates and time kinetics of the in vivo assembly of Escherichia coli ribosomes. J. Mol. Biol. 92:115–37
    [Google Scholar]
  81. 80.
    Lorenz C, Lünse C, Mörl M. 2017. tRNA modifications: impact on structure and thermal adaptation. Biomolecules 7:435
    [Google Scholar]
  82. 81.
    Luláková P, Perez-Mon C, Šantrůčková H, Ruethi J, Frey B 2019. High-alpine permafrost and active-layer soil microbiomes differ in their response to elevated temperatures. Front. Microbiol. 10:668
    [Google Scholar]
  83. 82.
    Luo C, Rodriguez-R LM, Johnston ER, Wu L, Cheng L et al. 2014. Soil microbial community responses to a decade of warming as revealed by comparative metagenomics. Appl. Environ. Microbiol. 80:51777–86
    [Google Scholar]
  84. 83.
    Ma DK, Li Z, Lu AY, Sun F, Chen S et al. 2015. Acyl-CoA dehydrogenase drives heat adaptation by sequestering fatty acids. Cell 161:51152–63
    [Google Scholar]
  85. 84.
    MacFadden DR, McGough SF, Fisman D, Santillana M, Brownstein JS. 2018. Antibiotic resistance increases with local temperature. Nat. Clim. Change 8:6510–14
    [Google Scholar]
  86. 85.
    Mackow ER, Chang FN. 1983. Correlation between RNA synthesis and ppGpp content in Escherichia coli during temperature shifts. Mol. Gen. Genet. 192:1–25–9
    [Google Scholar]
  87. 86.
    Magnusson LU, Farewell A, Nyström T. 2005. ppGpp: a global regulator in Escherichia coli. Trends Microbiol 13:5236–42
    [Google Scholar]
  88. 87.
    Manor H, Goodman D, Stent GS. 1969. RNA chain growth rates in Escherichia coli. J. Mol. Biol. 39:11–29
    [Google Scholar]
  89. 88.
    Marr AG, Ingraham JL. 1962. Effect of temperature on the composition of fatty acids in Escherichia coli. J. Bacteriol. 84:61260–67
    [Google Scholar]
  90. 89.
    Marsland R, Cui W, Mehta P. 2020. A minimal model for microbial biodiversity can reproduce experimentally observed ecological patterns. Sci. Rep. 10:3308
    [Google Scholar]
  91. 90.
    Maslak M, Martin CT. 1993. Kinetic analysis of T7 RNA polymerase transcription initiation from promoters containing single-stranded regions. Biochemistry 32:164281–85
    [Google Scholar]
  92. 91.
    McClure WR, Cech CL. 1978. On the mechanism of rifampicin inhibition of RNA synthesis. J. Biol. Chem. 253:248949–56
    [Google Scholar]
  93. 92.
    McClure WR, Jovin TM. 1975. The steady state kinetic parameters and non-processivity of Escherichia coli deoxyribonucleic acid polymerase I. J. Biol. Chem. 250:114073–80
    [Google Scholar]
  94. 93.
    Melillo JM, Frey SD, DeAngelis KM, Werner WJ, Bernard MJ et al. 2017. Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world. Science 358:6359101–5
    [Google Scholar]
  95. 94.
    Melillo JM, Steudler PA, Aber JD, Newkirk K, Lux H et al. 2002. Soil warming and carbon-cycle feedbacks to the climate system. Science 298:56012173–76
    [Google Scholar]
  96. 95.
    Michaels GA. 1972. Ribosome maturation of Escherichia coli growing at different growth rates. J. Bacteriol. 110:3889–94
    [Google Scholar]
  97. 96.
    Miguel A, Montón F, Li T, Gómez-Herreros F, Chávez S et al. 2013. External conditions inversely change the RNA polymerase II elongation rate and density in yeast. Biochim. Biophys. Acta Gene Regul. Mech. 1829:111248–55
    [Google Scholar]
  98. 97.
    Mihursky JA, McErlean AJ, Kennedy VS. 1970. Thermal pollution, aquaculture and pathobiology in aquatic systems. J. Wildl. Dis. 6:4347–55
    [Google Scholar]
  99. 98.
    Miller M, Pedersen JZ, Cox RP. 1988. Effect of growth temperature on membrane dynamics in a thermophilic cyanobacterium: a spin label study. Biochim. Biophys. Acta Biomembr. 943:3501–10
    [Google Scholar]
  100. 99.
    Mohr PW, Krawiec S. 1980. Temperature characteristics and Arrhenius plots for nominal psychrophiles, mesophiles and thermophiles. J. Gen. Microbiol. 121:2311–17
    [Google Scholar]
  101. 100.
    Monod J. 1949. The growth of bacterial cultures. Annu. Rev. Microbiol. 3:371–94
    [Google Scholar]
  102. 101.
    Monson RK, Burns SP, Williams MW, Delany AC, Weintraub M, Lipson DA 2006. The contribution of beneath-snow soil respiration to total ecosystem respiration in a high-elevation, subalpine forest. Global Biogeochem. Cycles 20:3GB3030
    [Google Scholar]
  103. 102.
    Mykytczuk NCS, Foote SJ, Omelon CR, Southam G, Greer CW, Whyte LG. 2013. Bacterial growth at −15°C: molecular insights from the permafrost bacterium Planococcus halocryophilus Or1. ISME J 7:61211–26
    [Google Scholar]
  104. 103.
    Nakashima H, Fukuchi S, Nishikawa K 2003. Compositional changes in RNA, DNA and proteins for bacterial adaptation to higher and lower temperatures. J. Biochem. 133:4507–13
    [Google Scholar]
  105. 104.
    Nguyen V, Wilson C, Hoemberger M, Stiller JB, Agafonov RV et al. 2017. Evolutionary drivers of thermoadaptation in enzyme catalysis. Science 355:6322289–94
    [Google Scholar]
  106. 105.
    Okabe K, Sakaguchi R, Shi B, Kiyonaka S. 2018. Intracellular thermometry with fluorescent sensors for thermal biology. Pflugers Arch. Eur. J. Physiol. 470:5717–31
    [Google Scholar]
  107. 106.
    Oshima T, Imahori K. 1974. Description of Thermus thermophilus (Yoshida and Oshima) comb. nov., a nonsporulating thermophilic bacterium from a Japanese thermal spa. Int. J. Syst. Bacteriol. 24:1102–12
    [Google Scholar]
  108. 107.
    Pace B, Campbell LL 1967. Correlation of maximal growth temperature and ribosome heat stability. PNAS 57:41110–16
    [Google Scholar]
  109. 108.
    Phillips R, Kondev J, Theriot J, Garcia HG, Orme N 2012. Physical Biology of the Cell New York: Garland Science
  110. 109.
    Pierucci O. 1972. Chromosome replication and cell division in Escherichia coli at various temperatures of growth. J. Bacteriol. 109:2848–54
    [Google Scholar]
  111. 110.
    Pietikäinen J, Pettersson M, Bååth E 2005. Comparison of temperature effects on soil respiration and bacterial and fungal growth rates. FEMS Microbiol. Ecol. 52:149–58
    [Google Scholar]
  112. 111.
    Raison JK. 1973. The influence of temperature-induced phase changes on the kinetics of respiratory and other membrane-associated enzyme systems. J. Bioenerg. 4:1–2285–309
    [Google Scholar]
  113. 112.
    Raison JK, Lyons JM, Mehlhorn RJ, Keith AD. 1971. Temperature-induced phase changes in mitochondrial membranes detected by spin labeling. J. Biol. Chem. 246:124036–40
    [Google Scholar]
  114. 113.
    Rao PN, Engelbero J. 1965. HeLa cells: effects of temperature on the life cycle. Science 38:1481092–94
    [Google Scholar]
  115. 114.
    Ratkowsky DA, Olley J, McMeekin TA, Ball A. 1982. Relationship between temperature and growth rate of bacterial cultures. J. Bacteriol. 149:11–5
    [Google Scholar]
  116. 115.
    Richter K, Haslbeck M, Buchner J. 2010. The heat shock response: life on the verge of death. Mol. Cell 40:2253–66
    [Google Scholar]
  117. 116.
    Ritchie ME. 2018. Reaction and diffusion thermodynamics explain optimal temperatures of biochemical reactions. Sci. Rep. 8:11105
    [Google Scholar]
  118. 117.
    Robinson JL, Pyzyna B, Atrasz RG, Henderson CA, Morrill KL et al. 2005. Growth kinetics of extremely halophilic Archaea (family Halobacteriaceae) as revealed by Arrhenius plots. J. Bacteriol. 187:3923–29
    [Google Scholar]
  119. 118.
    Rodnina MV, Pape T, Fricke R, Kuhn L, Wintermeyer W. 1996. Initial binding of the elongation factor Tu-GTP-aminoacyl-tRNA complex preceding codon recognition on the ribosome. J. Biol. Chem. 271:2646–52
    [Google Scholar]
  120. 119.
    Rodriguez-Correa D, Dahlberg AE. 2008. Kinetic and thermodynamic studies of peptidyltransferase in ribosomes from the extreme thermophile Thermus thermophilus. RNA 14:112314–18
    [Google Scholar]
  121. 120.
    Rodríguez-Verdugo A, Carrillo-Cisneros D, González-González A, Gaut BS, Bennett AF 2014. Different tradeoffs result from alternate genetic adaptations to a common environment. PNAS 111:3312121–26
    [Google Scholar]
  122. 121.
    Roe JH, Burgess RR, Record MT. 1984. Kinetics and mechanism of the interaction of Escherichia coli RNA polymerase with the λPR promoter. J. Mol. Biol. 176:4495–522
    [Google Scholar]
  123. 122.
    Roe JH, Burgess RR, Record MT. 1985. Temperature dependence of the rate constants of the Escherichia coli RNA polymerase-lambda PR promoter interaction: assignment of the kinetic steps corresponding to protein conformational change and DNA opening. J. Mol. Biol. 184:3441–53
    [Google Scholar]
  124. 123.
    Roszak DB, Colwell RR. 1987. Survival strategies of bacteria in the natural environment. Microbiol. Rev. 51:3365–79
    [Google Scholar]
  125. 124.
    Rudolph B, Gebendorfer KM, Buchner J, Winter J. 2010. Evolution of Escherichia coli for growth at high temperatures. J. Biol. Chem. 285:2519029–34
    [Google Scholar]
  126. 125.
    Ryals J, Little R, Bremer H. 1982. Temperature dependence of RNA synthesis parameters in Escherichia coli. J. Bacteriol. 151:2879–87
    [Google Scholar]
  127. 126.
    Saladino CF, Johnson HA. 1974. Rate of DNA synthesis as a function of temperature in cultured hamster fibroblasts (V-79) and HeLa-S3 cells. Exp. Cell Res. 85:2248–54
    [Google Scholar]
  128. 127.
    Satapathy SS, Dutta M, Ray SK 2010. Higher tRNA diversity in thermophilic bacteria: a possible adaptation to growth at high temperature. Microbiol. Res. 165:8609–16
    [Google Scholar]
  129. 128.
    Satapathy SS, Dutta M, Ray SK 2010. Variable correlation of genome GC% with transfer RNA number as well as with transfer RNA diversity among bacterial groups: α-proteobacteria and Tenericutes exhibit strong positive correlation. Microbiol. Res. 165:3232–42
    [Google Scholar]
  130. 129.
    Sawle L, Ghosh K. 2011. How do thermophilic proteins and proteomes withstand high temperature?. Biophys. J. 101:1217–27
    [Google Scholar]
  131. 130.
    Scalley ML, Baker D. 1997. Protein folding kinetics exhibit an Arrhenius temperature dependence when corrected for the temperature dependence of protein stability. PNAS 94:2010636–40
    [Google Scholar]
  132. 131.
    Schaechter M, Maaloe O, Kjeldgaard NO 1958. Dependency on medium and temperature of cell size and chemical composition during balanced growth of Salmonella typhimurium. J. Gen. Microbiol. 19:3592–606
    [Google Scholar]
  133. 132.
    Scholtissek C, Rott R. 1969. Effect of temperature on the multiplication of an influenza virus. J. Gen. Virol. 5:2283–90
    [Google Scholar]
  134. 133.
    Schroeder GK, Wolfenden R. 2007. The rate enhancement produced by the ribosome: an improved model. Biochemistry 46:134037–44
    [Google Scholar]
  135. 134.
    Scott M, Mateescu EM, Zhang Z, Hwa T. 2010. Interdependence of cell growth origins and consequences. Science 330:60071099–102
    [Google Scholar]
  136. 135.
    Seeton CJ. 2006. Viscosity-temperature correlation for liquids. Tribol. Lett. 22:167–78
    [Google Scholar]
  137. 136.
    Sells BH, Davis FC. 1968. Ribosome biogenesis: nonrandom addition of structural proteins to 50S subunits. Science 159:38201240–42
    [Google Scholar]
  138. 137.
    Shajani Z, Sykes MT, Williamson JR. 2011. Assembly of bacterial ribosomes. Annu. Rev. Biochem. 80:501–26
    [Google Scholar]
  139. 138.
    Sievers A, Beringer M, Rodnina MV, Wolfenden R. 2004. The ribosome as an entropy trap. PNAS 101:217897–901
    [Google Scholar]
  140. 139.
    Siliakus MF, van der Oost J, Kengen SWM. 2017. Adaptations of archaeal and bacterial membranes to variations in temperature, pH and pressure. Extremophiles 21:4651–70
    [Google Scholar]
  141. 140.
    Sinensky M. 1974. Homeoviscous adaptation: a homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli. PNAS 71:2522–25
    [Google Scholar]
  142. 141.
    Sizer IW 1943. Effects of temperature on enzyme kinetics. Advances in Enzymology and Related Areas of Molecular Biology, Vol. 3 FF Nord, CH Werkman 35–62 New York: Wiley
    [Google Scholar]
  143. 142.
    Solage A, Cedar H. 1976. The kinetics of E. coli RNA polymerase. Nucleic Acids Res 3:92207–22
    [Google Scholar]
  144. 143.
    Spencer-Martins I, Van Uden N. 1982. The temperature profile of growth, death and yield of the starch-converting yeast Lipomyces kononenkoae. Z. Allg. Mikrobiol. 22:7503–5
    [Google Scholar]
  145. 144.
    Sunagawa S, Coelho LP, Chaffron S, Kultima JR, Labadie K et al. 2015. Structure and function of the global ocean microbiome. Science 348:62371261359
    [Google Scholar]
  146. 145.
    Sykes J, Young TW. 1968. Studies on the ribosomes and ribonucleic acids of Aerobacter aerogenes grown at different rates in carbon-limited continuous culture. Biochim. Biophys. Acta Nucleic Acids Protein Synth. 169:1103–16
    [Google Scholar]
  147. 146.
    Tagkopoulos I, Liu Y-C, Tavazoie S. 2008. Predictive behavior within microbial genetic networks. Science 320:58811313–17
    [Google Scholar]
  148. 147.
    Talkington MWT, Siuzdak G, Williamson JR. 2005. An assembly landscape for the 30S ribosomal subunit. Nature 438:7068628–32
    [Google Scholar]
  149. 148.
    Tenaillon O, Rodríguez-Verdugo A, Gaut RL, McDonald P, Bennett AF et al. 2012. The molecular diversity of adaptive convergence. Science 335:6067457–61
    [Google Scholar]
  150. 149.
    Thompson MC, Barad BA, Wolff AM, Sun Cho H, Schotte F et al. 2019. Temperature-jump solution X-ray scattering reveals distinct motions in a dynamic enzyme. Nat. Chem. 11:111058–66
    [Google Scholar]
  151. 150.
    Towers NR, Raison JK, Kellerman GM, Linnane AW. 1972. Effects of temperature-induced phase changes in membranes on protein synthesis by bound ribosomes. Biochim. Biophys. Acta Nucleic Acids Protein Synth. 287:2301–11
    [Google Scholar]
  152. 151.
    Trgovčevic Ž, Kucan Ž. 1970. Is DNA polymerase involved in DNA degradation following ionizing radiation?. Nature 226:5247752–53
    [Google Scholar]
  153. 152.
    Újvári A, Martin CT. 1996. Thermodynamic and kinetic measurements of promoter binding by T7 RNA polymerase. Biochemistry 35:4614574–82
    [Google Scholar]
  154. 153.
    Uma S, Jadhav RS, Seshu Kumar G, Shivaji S, Ray MK 1999. A RNA polymerase with transcriptional activity at 0°C from the Antarctic bacterium Pseudomonas syringae. FEBS Lett 453:3313–17
    [Google Scholar]
  155. 154.
    Van De Vossenberg JLCM, Ubbink-Kok T, Elferink MGL, Driessen AJM, Konings WN. 1995. Ion permeability of the cytoplasmic membrane limits the maximum growth temperature of bacteria and archaea. Mol. Microbiol. 18:5925–32
    [Google Scholar]
  156. 155.
    VanBogelen RA, Neidhardt FC. 1990. Ribosomes as sensors of heat and cold shock in Escherichia coli. PNAS 87:155589–93
    [Google Scholar]
  157. 156.
    Vanoni M, Vai M, Frascotti G. 1984. Effects of temperature on the yeast cell cycle analyzed by flow cytometry. Cytometry 5:5530–33
    [Google Scholar]
  158. 157.
    Voges MJEEE, Bai Y, Schulze-Lefert P, Sattely ES. 2019. Plant-derived coumarins shape the composition of an Arabidopsis synthetic root microbiome. PNAS 116:2512558–65
    [Google Scholar]
  159. 158.
    Waldron C, Lacroute F. 1975. Effect of growth rate on the amounts of ribosomal and transfer ribonucleic acids in yeast. J. Bacteriol. 122:3855–65
    [Google Scholar]
  160. 159.
    Walter G, Zillig W, Palm P, Fuchs E. 1967. Initiation of DNA-dependent RNA synthesis and the effect of heparin on RNA polymerase. Eur. J. Biochem. 3:2194–201
    [Google Scholar]
  161. 160.
    Watanabe I, Okada S. 1967. Effects of temperature on growth rate of cultured mammalian cells (L5178Y). J. Cell Biol. 32:2309–23
    [Google Scholar]
  162. 161.
    Watanabe K, Shinma M, Oshima T, Nishimura S. 1976. Heat-induced stability of tRNA from an extreme thermophile, Thermus thermophilus. Biochem. Biophys. Res. Commun. 72:31137–44
    [Google Scholar]
  163. 162.
    Whitrow M. 1990. Wagner-Jauregg and fever therapy. Med. Hist. 34:3294–310
    [Google Scholar]
  164. 163.
    Wolfenden R, Snider M, Ridgway C, Miller B. 1999. The temperature dependence of enzyme rate enhancements. J. Am. Chem. Soc. 121:327419–20
    [Google Scholar]
  165. 164.
    Wowor AJ, Datta K, Brown HS, Thompson GS, Ray S et al. 2010. Thermodynamics of the DNA structural selectivity of the Pol I DNA polymerases from Escherichia coli and Thermusaquaticus. Biophys. J. 98:123015–24
    [Google Scholar]
  166. 165.
    Yergeau E, Kowalchuk GA 2008. Responses of Antarctic soil microbial communities and associated functions to temperature and freeze-thaw cycle frequency. Environ. Microbiol. 10:92223–35
    [Google Scholar]
  167. 166.
    Zakim D, Kavecansky J, Scarlata S. 1992. Are membrane enzymes regulated by the viscosity of the membrane environment?. Biochemistry 31:4611589–94
    [Google Scholar]
  168. 167.
    Zaritsky A. 1982. Effects of growth temperature on ribosomes and other physiological properties of Escherichia coli. J. Bacteriol. 151:1485–86
    [Google Scholar]
  169. 168.
    Zhu M, Dai X. 2019. Growth suppression by altered (p)ppGpp levels results from non-optimal resource allocation in Escherichia coli. Nucleic Acids Res. 47:94684–93
    [Google Scholar]
/content/journals/10.1146/annurev-biophys-112221-074832
Loading
/content/journals/10.1146/annurev-biophys-112221-074832
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error