THERMAL SCIENCE

International Scientific Journal

Authors of this Paper

External Links

Marko E. Popović

THERMODYNAMICS OF BACTERIA-PHAGE INTERACTIONS T4 AND LAMBDA BACTERIOPHAGES, AND E. COLI CAN COEXIST IN NATURAL ECOSYSTEMS DUE TO THE RATIO OF THEIR GIBBS ENERGIES OF BIOSYNTHESIS

ABSTRACT
The model of T4 phage, Lambda phage, and E. coli is often used in research on virus-host interactions. This paper reports for the first time the thermodynamic driving force of biosynthesis, catabolism and metabolism for the three organisms, on the M9 medium. Moreover, the influence of activities of nutrients and metabolic products is analyzed. All three organisms were found to have very similar Gibbs energies of metabolism. Moreover, since they share the same catabolism, their Gibbs energies of catabolism are identical. However, Gibbs energies of biosynthesis differ. The calculated thermodynamic properties have been used to explain the coexistence of both bacteria and phages in a dynamic equilibrium in natural ecosystems.
KEYWORDS
activity, driving force, metabolism, catabolism, environment
PAPER SUBMITTED: 2022-10-04
PAPER REVISED: 2022-11-25
PAPER ACCEPTED: 2022-12-02
PUBLISHED ONLINE: 2023-02-25
DOI REFERENCE: https://doi.org/10.2298/TSCI2301411P
CITATION EXPORT: view in browser or download as text file
THERMAL SCIENCE YEAR 2023, VOLUME 27, ISSUE Issue 1, PAGES [411 - 431]
REFERENCES
  1. Von Bertalanffy, L., The Theory of Open Systems in Physics and Biology. Science, 111 (1950), 2872, pp. 23-29
  2. Von Bertalanffy, L., General System Theory: Foundations, Development, Applications, George Braziller Inc., New York, USA, 1971
  3. Wimmer, E., The Test-Tube Synthesis of a Chemical Called Poliovirus. The Simple Synthesis of a Virus has Far-Reaching Societal Implications, EMBO reports, 7 (2006), Spec No., pp. S3-S9
  4. Von Stockar, U., Live Cells as Open Non-Equilibrium Systems, in: Biothermodynamics: The Role of Thermodynamics in Biochemical Engineering, EPFL Press, Lausanne, Switzerland, 2013, pp. 475-534
  5. Popovic, M., Thermodynamic Properties of Microorganisms: Determination and Analysis of Enthalpy, Entropy, and Gibbs Free Energy of Biomass, Cells and Colonies of 32 Microorganism Species, Heliyon, 5 (2019), 6, e01950
  6. Von Stockar, U., Biothermodynamics of Live Cells: Energy Dissipation and Heat Generation in Cellular Structures, in: Biothermodynamics: The Role of Thermodynamics in Biochemical Engineering, EPFL Press, Lausanne, Switzerland, 2013, pp. 475-534
  7. Ozilgen, M., Sorguven, E., Biothermodynamics: Principles and Applications, CRC Press, Boca Raton, Fla., USA, 2017
  8. Sandler, S. I., Chemical, Biochemical, and Engineering Thermodynamics, 5th ed., Wiley, Hoboken, N. J., USA, 2017
  9. Mahmoudabadi, G., et al., Energetic Cost of Building a Virus, PNAS, 114 (2017), 22, pp. E4324-E4333
  10. Yildiz, C., Ozilgen, M., Species-Specific Biological Energy Storage and Reuse, Energy Storage, 4 (2022), 6, e382
  11. Popovic, M., et al., Elemental Composition, Heat Capacity from 2 to 300 K and Derived Thermodynamic Functions of 5 Microorganism Species, J of Biotechnology, 331 (2021), Apr., pp. 99-107
  12. Molla, A., et al., Cell-Free, De Novo Synthesis of Poliovirus, Science, 254 (1991), 5038 pp. 1647-1651
  13. Popovic, M., Popovic, M., Strain Wars: Competitive Interactions Between SARS-Cov-2 Strains are Explained by Gibbs Energy of Antigen-Receptor Binding, Microbial Risk Analysis, 21 (2022), 100202
  14. Popovic, M., Strain Wars 2: Binding Constants, Enthalpies, Entropies, Gibbs Energies and Rates of Binding of SARS-CoV-2 Variants, Virology, 570 (2022), May, pp. 35-44
  15. Popovic, M., Strain wars 3: Differences in Infectivity and Pathogenicity Between Delta and Omicron Strains of SARS-CoV-2 can be Explained by Thermodynamic and Kinetic Parameters of Binding and Growth, Microbial Risk Analysis, 22 (2022), 100217
  16. Popovic, M., Atom Counting Method for Determining Elemental Composition of Viruses and its Applications in Biothermodynamics and Environmental Science, Computational Biology and Chemistry, 96 (2022), 107621
  17. Popovic, M., Strain Wars 4: Darwinian Evolution Through Gibbs' Glasses: Gibbs Energies of Binding and Growth Explain Evolution of SARS-CoV-2 from Hu-1 to BA.2, Virology, 575 (2022), Oct., pp. 36-42
  18. Popovic, M., Strain Wars 5: Gibbs Energies of Binding of BA.1 Through BA.4 Variants of SARS-CoV-2, Microbial Risk Analysis, 22 (2022), 100231
  19. Popovic, M., Beyond COVID-19: Do Biothermodynamic Properties Allow Predicting the Future Evolution of SARS-CoV-2 Variants?. Microbial Risk Analysis, 22 (2022), 100232
  20. Popovic, M., Formulas for Death and Life: Chemical Composition and Biothermodynamic Properties of Monkeypox (MPV, MPXV, HMPXV) and Vaccinia (VACV) viruses, Thermal Science, 26 (2022), 6A, pp. 4855-4868
  21. Popovic, M., Why doesn't Ebola Virus Cause Pandemics Like SARS-CoV-2? Microbial Risk Analysis, 22 (2022), 100236
  22. Simsek, B., et al., How Much Energy is Stored in SARS‐CoV‐2 and its Structural Elements? Energy Storage, 4 (2022), 2, e298
  23. Popovic, M., Minceva, M., Coinfection and Interference Phenomena are the Results of Multiple Thermodynamic Competitive Interactions, Microorganisms, 9 (2021), 10, 2060
  24. Maskow, T., et al., Calorimetric Real Time Monitoring of Lambda Prophage Induction, Journal of Virological Methods, 168 (2010), 1-2, pp. 126-132
  25. Guosheng, L., et al., Study on Interaction Between T4 Phage and Escherichia coli B by Microcalorimetric Method, Journal of Virological Methods, 112 (2003), 1-2, pp. 137-143
  26. Popovic, M., Minceva, M., A Thermodynamic Insight Into Viral Infections: Do Viruses in a Lytic Cycle Hijack Cell Metabolism Due to Their Low Gibbs Energy?, Heliyon, 6 (2003), 5, e03933
  27. Lavoisier, A. L., de Laplace, P. S., Memoir on Heat Read to the Royal Academy of Sciences, 28 june 1783, Obesity Research, 2 (1994), 2, pp. 189-202
  28. Muller, I., A History of Thermodynamics: The Doctrine of Energy and Entropy, Springer, Berlin, 2010
  29. Boltzmann, L., The Second Law of Thermodynamics, in: Theoretical Physics and Philosophical Problems, (ed., McGuinnes, B.,), D. Riedel Publishing Company, Boston, Mass., USA, 1974
  30. Popovic, M., Research in Entropy Wonderland: A Review of the Entropy Concept, Thermal Science, 22 (2018), 2, pp. 1163-1178
  31. Schrodinger, E., What is Life? The Physical Aspect of the Living Cell, Cambridge University Press, Cambridge, UK, 1944
  32. Glansdorff, P., Prigogine, I., Thermodynamic Theory of Structure, Stability and Fluctuations, Hoboken, Wiley, N. J., USA, 1971
  33. Prigogine, I., Wiame, J. M., Biology and Thermodynamics of Irreversible Phenomena (in French), Experientia, 2 (1946), Nov., pp. 451-453
  34. Prigogine, I., Thermodynamic Study of Irreversible Phenomena (in French), Dunod, Paris, 1947
  35. Prigogine, I., Nobel Lecture: Time, Structure and Fluctuations, Available at: www.nobelprize.org/prizes/chemistry/1977/prigogine/lecture/, 1977
  36. Popovic, M., Living Organisms from Prigogine's Perspective: An Opportunity to Introduce Students to Biological Entropy Balance, Journal of Biological Education, 52 (2018), 3, pp. 294-300
  37. Morowitz, H., The Emergence of Complexity, Complexity, 1 (1995), 1, pp. 4-5
  38. Morowitz, H. J., Beginnings of Cellular Life: Metabolism Recapitulates Biogenesis, Yale University Press, New Haven, Conn., USA, 1992
  39. Morowitz, H. J., Energy Flow in Biology: Biological Organization as a Problem in Thermal Physics, Academic Press, New York, USA, 1968
  40. Morowitz, H. J., Some Order-Disorder Considerations in Living Systems, Bulletin of Mathematical Biophysics, 17 (1955), June, pp. 81-86
  41. Morowitz, H. J., et al., The Origin of Intermediary Metabolism, Proceedings of the National Academy of Sciences, 97 (2000), 14, pp. 7704-7708
  42. Morowitz, H. J., et al., The Chemical Logic of a Minimum Protocell, Origins Life Evol Biosphere, 18 (1988), Sept., pp. 281-287
  43. von Stockar, U., Liu, J., Does Microbial Life Always Feed on Negative Entropy? Thermodynamic Analysis of Microbial Growth, Biochimica et Biophysica Acta, 1412 (1999), 3, pp. 191-211
  44. Von Stockar, U., et al., Thermodynamics of Microbial Growth and Metabolism: An Analysis of the Current Situation, Journal of Biotechnology, 121 (2006), 4, pp. 517-533
  45. von Stockar, U., et al., Can Microbial Growth Yield be Estimated Using Simple Thermodynamic Analogies to Technical Processes?. Chem. Eng. and Pro.: Pro. Intensification, 47 (2008), 6, pp. 980-990
  46. Patino, R., et al., A Study of the Growth for the Microalga Chlorella Vulgaris by Photo-Bio-Calorimetry and other On-Line and Off-Line Techniques, Biotechnology and Bioengineering, 96 (2007), 4, pp. 757-767
  47. Von Stockar, U., Marison, I. W., The Definition of Energetic Growth Efficiencies for Aerobic and Anaerobic Microbial Growth and their Determination by Calorimetry and by Other Means, Thermochimica Acta, 229 (1993), Dec., pp. 157-172
  48. Liu, J. S., et al., Microbial Growth by a Net Heat Up‐Take: A Calorimetric and Thermodynamic Study on Acetotrophic Methanogenesis by Methanosarcina Barkeri, Biotechnology and Bioengineering, 75 (2001), 2, pp. 170-180
  49. Hansen, L. D., et al., Transformation of Matter in Living Organisms During Growth and Evolution, Biophysical Chemistry, 271 (2021), 106550
  50. Hansen, L. D., et al., Laws of Evolution Parallel the Laws of Thermodynamics, The Journal of Chemical Thermodynamics, 124 (2018), Sept., pp. 141-148
  51. Hansen, L. D., et al., Biological Calorimetry and the Thermodynamics of the Origination and Evolution of Life, Pure and Applied Chemistry, 81 (2009), 10, pp. 1843-1855
  52. Lucia, U., Grisolia, G., How Life Works a Continuous Seebeck-Peltier Transition in Cell Membrane?. Entropy, 22 (2020), 9, 960
  53. Lucia, U., Bioengineering Thermodynamics of Biological Cells, Theoretical Biology & Medical Modelling, 12 (2015), 29
  54. Lucia, U., et al., A Thermoeconomic Indicator for the Sustainable Development with Social Considerations, Environ Dev Sustain, 24 (2022), May, pp. 2022-2036
  55. Grisolia, G., et al., The Education Index in the Context of Sustainability: Thermo-Economic Considerations, Frontiers in Physics, 10 (2022), Aug., 800
  56. Lucia, U., Grisolia, G., The Gouy-Stodola Theorem from Irreversibility to Sustainability the Thermodynamic Human Development Index, Sustainability, 13 (2021), 7, 3995
  57. Maskow, T., et al., What Heat is Telling us About Microbial Conversions in Nature and Technology: from Chip- to Megacalorimetry, Microbial Biotechnology, 3 (2010), 3, pp. 269-284
  58. Maskow, T., Paufler, S., What does Calorimetry and Thermodynamics of Living Cells Tell Us?. Methods, 76 (2015), Apr., pp. 3-10
  59. Maskow, T., Harms, H., Real Time Insights Into Bioprocesses Using Calorimetry: State of the Art and Potential, Engineering in Life Sciences, 6 (2006), 3, pp. 266-277
  60. Maskow, T., von Stockar, U., How Reliable are Thermodynamic Feasibility Statements of Biochemical Pathways?. Biotechnology and Bioengineering, 92 (2005), 2, pp. 223-230
  61. Maskow, T., Miniaturization of Calorimetry: Strengths and Weaknesses for Bioprocess Monitoring, in: Biothermodynamics: The Role of Thermodynamics in Biochemical Engineering, (ed. von Stockar, U.,), EPFL Press, Lausanne, Switzerland, 2013, pp. 423-442
  62. Korth, B., et al., Precious Data from Tiny Samples: Revealing the Correlation Between Energy Content and the Chemical Oxygen Demand of Municipal Wastewater by Micro-Bomb Combustion Calorimetry, Frontiers in Energy Research, 9 (2021), 705800
  63. Fricke, C., et al., Rapid Calorimetric Detection of Bacterial Contamination: Influence of the Cultivation Technique, Frontiers in Microbiology, 10 (2019), Nov., 2530
  64. Barros, N., et al., The Effect of Extreme Temperatures on Soil Organic Matter Decomposition from Atlantic Oak Forest Ecosystems, Iscience, 24 (2021), 12, 103527
  65. Barros, N., Thermodynamics of Soil Microbial Metabolism: Applications and Functions, Applied Sciences, 11 (2021), 11, 4962
  66. Barros, N., et al., Thermodynamics of Soil Organic Matter Decomposition in Semi-Natural Oak (Quercus) Woodland in Southwest Ireland, Oikos, 129 (2020), 11, pp. 1632-1644
  67. Barros, N., et al., Factors Influencing the Calorespirometric Ratios of Soil Microbial Metabolism, Soil Biology and Biochemistry, 92 (2016). Jan., pp. 221-229
  68. Xu, J., et al., Exploring the Potential of Microcalorimetry to Study Soil Microbial Metabolic Diversity, Journal of Thermal Analysis and Calorimetry, 127 (201), 2, pp. 1457-1465
  69. Berg, J. M., et al., Biochemistry, 5th ed.. Freeman, New York, USA, (Section 14.1, Metabolism Is Composed of Many Coupled, Interconnecting Reactions, 2002
  70. Gale, P., Using Thermodynamic Equilibrium Models to Predict the Effect of Antiviral Agents on Infectivity: Theoretical Application to SARS-CoV-2 and Other Viruses, Microbial Risk Analysis, 21 (2022), 100198
  71. Gale, P., How Virus Size and Attachment Parameters Affect the Temperature Sensitivity of Virus Binding to Host Cells: Predictions of a Thermodynamic Model for Arboviruses and HIV, Microbial Risk Analysis, 15 (2020), 100104
  72. Gale, P., Towards a Thermodynamic Mechanistic Model for the Effect of Temperature on Arthropod Vector Competence for Transmission of Arboviruses, Microbial Risk Analysis, 12 (2019), Aug., pp. 27-43
  73. Gale, P., Using Thermodynamic Parameters to Calibrate a Mechanistic Dose-Response for Infection of a Host by a Virus, Microbial risk analysis, 8 (2018), Apr., pp. 1-13
  74. Lucia, U., et al., Thermodynamics and SARS-CoV-2: Neurological Effects in Post-Covid 19 Syndrome. Atti della Accademia Peloritana dei Pericolanti, 99 (2021), 2, A3
  75. Lucia, U., et al., Seebeck-Like Effect in SARS-CoV-2 Bio-Thermodynamics, Atti della Accademia Peloritana dei Pericolanti-Classe di Scienze Fisiche, Matematiche e Naturali, 98 (2020), 2, 6
  76. Lucia, U., et al., Entropy-Based Pandemics Forecasting, Frontiers in Physics, 8 (2020), 274
  77. Kaniadakis, G., et al., The κ-Statistics Approach to Epidemiology, Scientific Reports, 10 (2020), 1, 19949
  78. Privalov, P. L., Microcalorimetry of Macromolecules: The Physical Basis of Biological Structures, John Wiley & Sons, Hoboken, N. J., USA, 2012
  79. Sarge, S. M., et al., Calorimetry: Fundamentals, Instrumentation and Applications, John Wiley & Sons, Hoboken, N, J., USA, 2014
  80. Bauer, D. W., et al., Exploring the Balance between DNA Pressure and Capsid Stability in Herpesviruses and Phages, Journal of Virology, 89 (2015), 18, pp. 9288-9298
  81. Bauer, D. W., Evilevitch, A., Influence of Internal DNA Pressure on Stability and Infectivity of Phage λ, Journal of Molecular Biology, 427 (2015), 20, pp. 3189-3200
  82. Li, D., et al., Ionic Switch Controls the DNA State in Phage λ, Nucleic Acids Research, 43 (2015), 13, pp. 6348-6358
  83. Evilevitch, A.,The Mobility of Packaged Phage Genome Controls Ejection Dynamics, eLife, 7 (2018), Sept., e37345
  84. Chakraborty, S., et al., Mechanistic Insight into the Structure and Dynamics of Entangled and Hydrated λ-Phage DNA, The Journal of Physical Chemistry. A, 116 (2012), 17, pp. 4274-4284
  85. Petsong, K., et al., Optimization of Wall Material for Phage Encapsulation via Freeze-Drying and Antimicrobial Efficacy of Microencapsulated Phage against Salmonella, Journal of Food Science and Technology, 58 (2021), 5, pp. 1937-1946
  86. Chang, R. Y. K., et al., Storage Stability of Inhalable Phage Powders Containing Lactose at Ambient Conditions, International Journal of Pharmaceutics, 560 (2019), Apr., pp. 11-18
  87. Zhang, Y., et al., The Stabilizing Excipients in Dry State Therapeutic Phage Formulations, AAPS PharmSciTech, 21 (2020), 4, 133
  88. Leung, S. S., et al., Production of Inhalation Phage Powders Using Spray Freeze Drying and Spray Drying Techniques for Treatment of Respiratory Infections, Pharmaceutical Research, 33 (2016), 6, pp. 1486-1496
  89. Malik, D. J., Bacteriophage Encapsulation Using Spray Drying for Phage Therapy, Current Issues in Molecular Biology, 40 (2021), pp. 303-316
  90. Lerchner, J., et al., Chip-Calorimetric Evaluation of the Efficacy of Antibiotics and Bacteriophages Against Bacteria on a Minute-Timescale, J. of Therm. Ana. and Calorimetry, 104 (2011), 1, pp. 31-36
  91. Morais, F. M., et al., Chip-Calorimetric Monitoring of Biofilm Eradication with Bacteriophages Reveals an Unexpected Infection-Related Heat Profile, J. of Therm. Ana. and Cal., 115 (2014), 3, pp. 2203-2210
  92. Tkhilaishvili, T., et al., Real-Time Assessment of Bacteriophage T3-Derived Antimicrobial Activity Against Planktonic and Biofilm-Embedded Escherichia Coli by Isothermal Microcalorimetry, Research in Microbiology, 169 (2018), 9, pp. 515-521
  93. Wang, L., et al., Bacteriophage-Antibiotic Combinations Against Ciprofloxacin/Ceftriaxone-Resistant Escherichia Coli in Vitro and in an Experimental Galleria Mellonella Model, International Journal of Antimicrobial Agents, 56 (2020), 6, 106200
  94. Tkhilaishvili, T., et al., Using Bacteriophages as a Trojan Horse to the Killing of Dual-Species Biofilm Formed by Pseudomonas Aeruginosa and Methicillin Resistant Staphylococcus Aureus, Frontiers in Microbiology, 11 (2020), 695
  95. Tkhilaishvili, T., et al., Antibacterial Efficacy of Two Commercially Available Bacteriophage Formulations, Staphylococcal Bacteriophage and PYO Bacteriophage, Against Methicillin-Resistant Staphylococcus aureus: Prevention and Eradication of Biofilm Formation and Control of a Systemic Infection of Galleria mellonella Larvae, Frontiers in Microbiology, 11 (2020), 110
  96. Tkhilaishvili, T., et al., Bacteriophage Sb-1 Enhances Antibiotic Activity Against Biofilm, Degrades Exopolysaccharide Matrix And Targets Persisters of Staphylococcus Aureus, International Journal of Antimicrobial Agents, 52 (2018), 6, pp. 842-853
  97. Tkhilaishvili, T., et al., Simultaneous and Sequential Applications of Phages and Ciprofloxacin in Killing Mixed-Species Biofilm of Pseudomonas Aeruginosa and Staphylococcus Aureus, in: Orthopaedic Proceedings, The British Editorial Society of Bone & Joint Surgery, London, UK, Vol. 100, No. Suppl. 17, pp. 65-65, 2018
  98. Mariana, F., Chip-Calorimetric Monitoring and Biothermodynamic Analysis of Biofilm Growth and Interactions with Chemical and Biological Agents, Ph. D. thesis, Technical University of Dresden, Dresden, Germany, 2015
  99. Qiu, X., Heat Induced Capsid Disassembly and DNA Release of Bacteriophage λ, PloS one, 7 (2012), 7, e39793
  100. Chang, R. Y. K., et al., Inhalable Bacteriophage Powders: Glass Transition Temperature and Bioactivity Stabilization, Bioengineering & Translational Medicine, 5 (2020), 2, e10159
  101. Boggione, D. M. G., et al., Preparation of Polyvinyl Alcohol Hydrogel Containing Bacteriophage and Its Evaluation for Potential Use in the Healing of Skin Wounds, Journal of Drug Delivery Science and Technology, 63 (2021), 102484
  102. Heselpoth, R. D., et al., Quantitative Analysis of the Thermal Stability of the Gamma Phage Endolysin Plyg: A Biophysical and Kinetic Approach to Assaying Therapeutic Potential, Virology, 477 (2015), Mar., pp. 125-132
  103. Xu, J., et al., An Enhanced Bioindicator for Calorimetric Monitoring of Prophage-Activating Chemicals in the Trace Concentration Range, Engineering in Life Sciences, 18 (2018), 7, pp. 475-483
  104. Kurochkina, L. P., et al., Expression and Functional Characterization of the First Bacteriophage-Encoded Chaperonin, Journal of Virology, 86 (2012), 18, pp. 10103-10111
  105. Lee, S. J., et al., Residues of Escherichia coli Thioredoxin Critical for Interaction with Phage T7 DNA Polymerase to Increase Processivity, The FASEB Journal, 31 (2017), S1, 592-3
  106. Plotka, M., et al., Biochemical Characterization and Validation of a Catalytic Site of a Highly Thermostable Ts2631 Endolysin from the Thermus Scotoductus Phage vB_Tsc2631, PloS one, 10 (2015), 9, e0137374
  107. Lee, J.-M., et al., Improvement of High Affinity and Selectivity on Biosensors Using Genetically Engineered Phage by Binding Isotherm Screening, Viruses, 11 (2019), 3, 248
  108. Popovic, M., Minceva, M., Thermodynamic Insight Into Viral Infections 2: Empirical Formulas, Molecular Compositions and Thermodynamic Properties of SARS, MERS and SARS-CoV-2 (COVID-19) Viruses, Heliyon, 6 (2020), 9, e04943
  109. Patel, S. A., Erickson, L. E., Estimation of Heats of Combustion of Biomass from Elemental Analysis Using Available Electron Concepts, Biotechnology and Bioengineering, 23 (1981), 9, pp. 2051-2067
  110. Battley E. H., A Theoretical Study of the Thermodynamics of Microbial Growth Using Saccharomyces Cerevisiae and a Different Free Energy Equation, The Quarterly Review of Biology, 88 (2013), 2, pp. 69-96
  111. Battley, E. H., An Empirical Method for Estimating the Entropy of Formation and the Absolute Entropy of Dried Microbial Biomass for use in Studies on the Thermodynamics of Microbial Growth, Thermochimica Acta, 326 (1999), 1-2, pp. 7-15
  112. Battley, E. H., The Development of Direct and Indirect Methods for the Study of the Thermodynamics of Microbial Growth. Thermochimica Acta, 309 (1998), 1-2, pp. 17-37
  113. Battley, E. H., On the Enthalpy of Formation of Escherichia coli K‐12 cells, Biotechnology and Bioengineering, 39 (1992), 1, pp. 5-12
  114. Bauer, S., Ziv, E., Dense Growth of Aerobic Bacteria in a Bench‐Scale Fermentor, Biotechnology and Bioengineering, 18 (1976), 1, pp. 81-94
  115. Geerlof, A., M9 Mineral Medium, Helmholtz Center Munich, available at: www.helmholtz-muenchen.de/fileadmin/PEPF/Protocols/M9-medium_150510.pdf, 2010
  116. ***, Cold Spring Harbor Protocols, M9 Minimal Medium (standard), Cold Spring Harbor Laboratory, available at: doi.org/10.1101/pdb.rec12295, 2022
  117. Xing, W., et al., Oxygen Solubility, Diffusion Coefficient, and Solution Viscosity, in: Rotating Electrode Methods and Oxygen Reduction Electrocatalysts, Elsevier, Amsterdam, The Netherlands, 2014, pp. 1-31
  118. Atkins, P. W., de Paula, J., Physical Chemistry for the Life Sciences, 2nd ed., W. H. Freeman and Company, New York, USA, 2011
  119. Atkins, P. W., de Paula, J., Physical Chemistry: Thermodynamics, Structure, and Change, 10th ed., W. H. Freeman and Company, New York, USA, 2014
  120. Rard, J. A., Wolery, T. J., The Standard Chemical-Thermodynamic Properties of Phosphorus and Some of its Key Compounds and Aqueous Species: An Evaluation of Differences between the Previous Recommendations of NBS/NIST and CODATA, J. of Solution Chem., 36 (2007), 11-12, pp. 1585-1599
  121. Kielland, J., Individual Activity Coefficients of Ions in Aqueous Solutions, Journal of the American Chemical Society, 59 (1937), 9, pp. 1675-1678
  122. Skoog, D. A., et al., Fundamentals of Analytical Chemistry, 9th ed., Cengage Learning, Boston, Mass., USA, 2013
  123. Popovic, M., Omicron BA.2.75 Sublineage (Centaurus) Follows the Expectations of the Evolution Theory: Less Negative Gibbs Energy of Biosynthesis Indicates Decreased Pathogenicity, Microbiology Research, 13 (2022), 4, pp. 937-952
  124. Heijnen, J. J., A Thermodynamic Approach to the Black Box Model, in:, Biothermodynamics: The Role of Thermodynamics in Biochemical Engineering, (ed. Urs von Stockar), EPFL Press, Lausanne, Switzerland, 2013, pp. 443-473
  125. Heijnen, J. J., Van Dijken, J. P., In Search of a Thermodynamic Description of Biomass Yields for the Chemotrophic Growth of Microorganisms, Biotechnology and Bioengineering, 39 (1992), 8, pp. 833-858
  126. Liu, J. S., et al., A Comparison of Various Gibbs Energy Dissipation Correlations for Predicting Microbial Growth Yields, Thermochimica Acta, 458 (2007), 1-2, pp. 38-46
  127. Roels, J. A., Energetics and Kinetics in Biotechnology, Elsevier, Amsterdam, The Netherlands, 1983
  128. Von Stockar, U., et al., Thermodynamic Analysis of Metabolic Pathways, in: Biothermodynamics: the Role of Thermodynamics in Biochemical Engineering, (ed. von Stockar, U.,) EPFL Press, Lausanne, Switzerland, 2013, pp. 581-604
  129. Popovic, M., et al., Thermodynamics of Hydrolysis of Cellulose to Glucose from 0 to 100 C°: Cellulosic Biofuel Applications and Climate Change Implications, The Journal of Chemical Thermodynamics, 128 (2019), Jan., pp. 244-250
  130. Popovic, M., Biothermodynamic Key Opens the Door of Life Sciences: Bridging the Gap between Biology and Thermodynamics, Preprints, doi.org/10.20944/preprints202210.0326.v1, 2022
  131. Popovic, M., Biothermodynamics of Viruses from Absolute Zero (1950) To - Virothermodynamics (2020), Vaccines, 10 (2022), 12, 2112
  132. Demirel, Y., Nonequilibrium Thermodynamics: Transport and Rate Processes in Physical, Chemical and Biological Systems, 3rd ed., Elsevier, Amsterdam, The Netherlands, 2014
  133. Hellingwerf, K. J., et al., Energetics of Microbial Growth: An Analysis of the Relationship Between Growth and its Mechanistic Basis by Mosaic Non‐Equilibrium Thermodynamics, FEMS Microbiology Letters, 15 (1982), 1, pp. 7-17
  134. Westerhoff, H. V., et al., Thermodynamics of Growth. Non-Equilibrium Thermodynamics of Bacterial Growth: The Phenomenological and the Mosaic Approach, Biochimica et Biophysica Acta (BBA) - Reviews on Bioenergetics, 683 (1982), 3-4, pp. 181-220
  135. De Paepe, M., Petit, M. A., Phage Predation: Killing the killers, eLife, 3 (2014), e04168
  136. Jover, L. F., et al., The Elemental Composition of Virus Particles: Implications for Marine Biogeochemical Cycles, Nature Reviews. Microbiology, 12 (2014), 7, pp. 519-528
PDF VERSION [DOWNLOAD]
Thermodynamics of bacteria-phage interactions T4 and Lambda bacteriophages, and E. coli can coexist in natural ecosystems due to the ratio of their Gibbs energies of biosynthesis

© 2024 Society of Thermal Engineers of Serbia. Published by the Vinča Institute of Nuclear Sciences, National Institute of the Republic of Serbia, Belgrade, Serbia. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International licence