THERMAL SCIENCE

International Scientific Journal

Thermal Science - Online First

Marko E. Popović

,

Gavrilo Šekularac

,

Vojin Tadić

,

Marijana Pantović-Pavlović

online first only

The silent assassin: Empirical formulas, molar masses, biosynthesis reactions, enthalpies, entropies and Gibbs energies of biosynthesis and Gibbs energies of binding of Coxsackieviruses A and B

ABSTRACT
Coxsackievirus B represents a nightmare for a large number of medical staff. Due to exposure to Coxsackievirus in closed spaces (ambulances and waiting rooms), infections by Coxsackievirus B are a common occurrence. This paper for the first time reports chemical and thermodynamic properties of Coxsackieviruses A and B, and offers a mechanistic model of Coxsackievirus-host interaction. The driving force of the interaction at the membrane (antigen-receptor binding) is Gibbs energy of binding. The driving force of virus-host interaction in the cytoplasm is Gibbs energy of biosynthesis. This paper analyzes the mechanism of hijacking of cell metabolic machinery of susceptible cells.
KEYWORDS
Biothermodynamics, Bioenergetics, Virus-host interaction, Infectivity, Pathogenicity, Virus multiplication, Permissiveness, Susceptibility, Microorganism, Infection
PAPER SUBMITTED: 2024-04-29
PAPER REVISED: 2024-07-01
PAPER ACCEPTED: 2024-07-08
PUBLISHED ONLINE: 2024-10-12
DOI REFERENCE: https://doi.org/10.2298/TSCI240429213P
REFERENCES
  1. Cantor, D., Reinventing Hippocrates, 1st ed., Routledge, London, UK, 2014
  2. Casadevall, A., Pirofski, L. A., Host-pathogen interactions: basic concepts of microbial commensalism, colonization, infection, and disease, Infection and immunity, 68 (2000), 12, pp. 6511-6518.
  3. Shors, T., Understanding viruses, 1st ed., Jones & Bartlett Learning, Burlington, MA, 2008
  4. 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
  5. 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
  6. Morowitz, H.J., Beginnings of Cellular Life: Metabolism Recapitulates Biogenesis, Yale University Press, New Haven, CT, USA, 1992
  7. Morowitz, H.J., Energy Flow in Biology: Biological Organization as a Problem in Thermal Physics. Academic Press, New York, USA, 1968
  8. Von Stockar, U., Live cells as open non-equilibrium systems, in Biothermodynamics: The Role of Thermodynamics in Biochemical Engineering (Ed. U. von Stockar), EPFL Press, Lausanne, Switzerland, 2013, pp. 399-421
  9. Von Stockar, U., Biothermodynamics of live cells: energy dissipation and heat generation in cellular structures, in Biothermodynamics: The Role of Thermodynamics in Biochemical Engineering (Ed. U. von Stockar), EPFL Press, Lausanne, Switzerland, 2013, pp. 475-534
  10. Assael, M.J. et al., Commonly Asked Questions in Thermodynamics, 2nd ed., CRC Press, Boca Raton, FL, USA, 2022. ISBN: 9780367338916
  11. 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
  12. Molla, A., et al., Cell-free, de novo synthesis of poliovirus, Science, 254 (1991), 5038, pp. 1647-1651
  13. Popovic, M., Comparative study of entropy and information change in closed and open thermodynamic systems, Thermochimica Acta, 598 (2014), pp. 77-81
  14. Popovic, M., Entropy change of open thermodynamic systems in self-organizing processes. Thermal Science, 18 (2014), 4, pp. 1425-1432
  15. Şimşek, B., et al., How much energy is stored in SARS‐CoV‐2 and its structural elements?. Energy Storage, 4 (2021), 2, pp. e298
  16. Degueldre, C., Single virus inductively coupled plasma mass spectroscopy analysis: A comprehensive study. Talanta, 228 (2021), pp. 122211
  17. Popović, M.E, et al., Eris - another brick in the wall: Empirical formulas, molar masses, biosynthesis reactions, enthalpy, entropy and Gibbs energy of Omicron EG.5 Eris and EG.5.1 variants of SARS-CoV-2, Microbial Risk Analysis, 25 (2023), pp. 100280
  18. Popovic, M.E., et al., Upcoming epidemic storm: Empirical formulas, biosynthesis reactions, thermodynamic properties and driving forces of multiplication of the omicron XBB.1.9.1, XBF and XBB.1.16 (Arcturus) variants of SARS-CoV-2, Microbial Risk Analysis, 25 (2023), pp. 100273
  19. Popovic, M., et al., Ghosts of the past: Elemental composition, biosynthesis reactions and thermodynamic properties of Zeta P.2, Eta B.1.525, Theta P.3, Kappa B.1.617.1, Iota B.1.526, Lambda C.37 and Mu B.1.621 variants of SARS-CoV-2, Microbial risk analysis, 24 (2023), pp. 100263
  20. Popovic, M., SARS-CoV-2 strain wars continues: Chemical and thermodynamic characterization of live matter and biosynthesis of Omicron BN.1, CH.1.1 and XBC variants, Microbial Risk Analysis, 24 (2023), pp. 100260
  21. Popovic, M., XBB.1.5 Kraken cracked: Gibbs energies of binding and biosynthesis of the XBB.1.5 variant of SARS-CoV-2, Microbiological Research, 270 (2023), pp. 127337
  22. Popovic, M., Never ending story? Evolution of SARS-CoV-2 monitored through Gibbs energies of biosynthesis and antigen-receptor binding of Omicron BQ.1, BQ.1.1, XBB and XBB.1 variants, Microbial Risk Analysis, 23 (2023), pp. 100250
  23. 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
  24. Popovic, M., Beyond COVID-19: Do biothermodynamic properties allow predicting the future evolution of SARS-CoV-2 variants?, Microbial Risk Analysis, 22 (2022), pp. 100232
  25. 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), pp. 36-42
  26. 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), pp. 100217
  27. Popovic, M., Why doesn't Ebola virus cause pandemics like SARS-CoV-2?, Microbial Risk Analysis, 22 (2022), pp. 100236
  28. 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
  29. Popovic, M., et al., Death from the Nile: Empirical formula, molar mass, biosynthesis reaction and Gibbs energy of biosynthesis of the West Nile virus, Microbial Risk Analysis, 25 (2023), pp. 100281
  30. Popovic, M., 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, Thermal Science, 27 (2023), 1, pp. 411-431
  31. 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, Helyon, 5 (2019), 6, pp. e01950
  32. Popovic, M., et al., Thermodynamics of microbial consortia: Enthalpies and Gibbs energies of microorganism live matter and macromolecules of E. coli, G. oxydans, P. fluorescens, S. thermophilus and P. chrysogenum, Journal of Biotechnology, 379 (2024), pp. 6-17
  33. Popović, M.E., et al., Return of the forgotten nightmare: Bordetella pertussis uses a more negative Gibbs energy of metabolism to outcompete its host organism, Microbial Risk Analysis, 26 (2024), pp. 100292
  34. Popovic, M., et al., Elemental composition, heat capacity from 2 to 300 K and derived thermodynamic functions of 5 microorganism species, Journal of Biotechnology, 331 (2021), pp. 99-107
  35. Patiño, 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
  36. Popovic, M., Minceva, M., Standard thermodynamic properties, biosynthesis rates and the driving force of growth of 5 agricultural plants, Frontiers in Plant Science, 12 (2021), pp. 871
  37. Dragičević, V., et al., Energy distribution between maize and weeds, in Proceedings of the 15th International conference on fundamental and applied aspects of physical chemistry, Belgrade, 20-24.09. 2021. (Vol. 2), Society of physical chemists of Serbia, Belgrade, Serbia, pp. 681-684
  38. Dragicevic, V., Sredojevic, S., Thermodynamics of Seed and Plant Growth, InTech, Rijeka, Croatia, 2011
  39. Popović, M.E., et al., Chemical and thermodynamic properties of Bombyx mori (domestic silk moth): Empirical formula, driving force, and biosynthesis, catabolism and metabolism reactions, Thermal Science, 27 (2023), 6B, pp. 4893-4910
  40. Popovic, M., Animal bioenergetics: Thermodynamic and kinetic analysis of growth and metabolism of Anguilla anguilla, Zoology, 163 (2024), pp. 126158
  41. Popovic, M.E., Minceva, M., Thermodynamic properties of human tissues, Thermal Science, 24 (2020), 6B, pp. 4115-4133
  42. Popovic, M., et al., From genotype to phenotype with biothermodynamics: Empirical formulas, biosynthesis reactions and thermodynamic properties of preproinsulin, proinsulin and insulin molecules, Journal of Biomolecular Structure & Dynamics, (2023), doi.org/10.1080/07391102.2023.2256880
  43. Popović, M., et al., Breaking news: Empirical formulas, molar masses, biosynthesis reactions, and thermodynamic properties of virus particles, biosynthesis and binding of Omicron JN.1 variant of SARS-CoV-2, Journal of the Serbian Chemical Society, 89 (2024), 3, pp. 305-320
  44. Popovic, M., Biothermodynamics of Viruses from Absolute Zero (1950) To - Virothermodynamics (2022), Vaccines, 10 (2022), 12, pp. 2112
  45. Popović, M.E. et al., Like a summer storm: Biothermodynamic analysis of Rotavirus A - Empirical formula, biosynthesis reaction and driving force of virus multiplication and antigen-receptor binding, Microbial Risk Analysis, 26 (2024), pp. 100291
  46. Du, X., et al., Insights into protein-ligand interactions: mechanisms, models, and methods, International journal of molecular sciences, 17 (2016), 2, pp. 144
  47. 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), pp. 100198
  48. 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), pp. 100104
  49. Popović, M.E., et al., The wind of change: Gibbs energy of binding and infectivity evolution of Omicron BA.2.86 Pirola, EG.5.1, XBB.1.16 Arcturus, CH.1.1 and BN.1 variants of SARS-CoV-2, Microbial Risk Analysis, 26 (2024), pp. 100290
  50. Popovic, M, et al., COVID infection in 4 steps: Thermodynamic considerations reveal how viral mucosal diffusion, target receptor affinity and furin cleavage act in concert to drive the nature and degree of infection in human COVID-19 disease, Heliyon, 9 (2023), 6, pp. e17174
  51. Popovic, M., The SARS-CoV-2 Hydra, a monster from the 21st century: Thermodynamics of the BA.5.2 and BF.7 variants, Microbial Risk Analysis, 23 (2023), pp. 100249
  52. Popovic, M., Omicron BA.2.75 subvariant of SARS-CoV-2 is expected to have the greatest infectivity compared with the competing BA.2 and BA.5, due to most negative Gibbs energy of binding, BioTech, 11 (2022), 4, pp. 45
  53. 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), pp. 100231
  54. Popovic, M., Strain wars 2: Binding constants, enthalpies, entropies, Gibbs energies and rates of binding of SARS-CoV-2 variants, Virology, 570 (2022), pp. 35-44
  55. 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), pp. 100202
  56. Pinheiro, A.V., et al., Light activation of transcription: photocaging of nucleotides for control over RNA polymerization, Nucleic acids research, 36 (2008), 14, pp. e90
  57. Lee, J., et al., Ribosome-mediated polymerization of long chain carbon and cyclic amino acids into peptides in vitro, Nature communications, 11 (2020), 1, pp. 4304
  58. Dodd, T., et al., Polymerization and editing modes of a high-fidelity DNA polymerase are linked by a well-defined path. Nat Commun, 11 (2020), pp. 5379
  59. Johansson, E., Dixon, N., Replicative DNA polymerases, Cold Spring Harbor perspectives in biology, 5 (2013), 6, pp. a012799
  60. Balmer, R.T., Modern Engineering Thermodynamics, Academic Press, Cambridge, MA, USA, 2010
  61. 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
  62. Clausius, R, The Mechanical Theory of Heat - with its Applications to the Steam Engine and to Physical Properties of Bodies, John van Voorst, London, UK, 1867
  63. Clausius, R., On a Mechanical Theorem Applicable to Heat, Philosophical Magazine Series 4, 40 (1870), 265, pp. 122
  64. Clausius, R., On different forms of the fundamental equations of the mechanical theory of heat and their convenience for application, in: The Second Law of Thermodynamics (Ed. J. Kestin), Dowen, Hutchingson and Ross, Inc., Stroudsburg, PA, USA, 1976
  65. Müller, I., A History of Thermodynamics: The Doctrine of Energy and Entropy, Springer, Berlin, Germany, 2010
  66. Popovic, M., Researchers in an Entropy Wonderland: A Review of the Entropy Concept, arXiv, (2017), pp. arXiv:1711.07326. arxiv.org/abs/1711.07326
  67. Hansen, L. D., et al. Transformation of matter in living organisms during growth and evolution, Biophysical Chemistry, 271 (2021), pp. 106550
  68. Hansen, L. D., et al., Laws of evolution parallel the laws of thermodynamics, The Journal of Chemical Thermodynamics, 124 (2018), pp. 141-148
  69. 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
  70. Lucia, U., Statistical approach of the irreversible entropy variation, Physica A: Statistical Mechanics and its Applications, 387 (2008)., 14, pp. 3454-3460. doi.org/10.1016/j.physa.2008.02.002
  71. Lucia, U., Thermodynamic approach to nano-properties of cell membrane, Physica A: Statistical Mechanics and its Applications, 407 (2014), pp. 185-191. doi.org/10.1016/j.physa.2014.03.075
  72. Grisolia, G., et al., Thermodynamic optimisation of the biofuel production based on mutualism, Energy Reports, 6 (2020), 1561-1571. doi.org/10.1016/j.egyr.2020.06.014
  73. Lucia, U., Grisolia, G., Cyanobacteria and Microalgae: Thermoeconomic Considerations in Biofuel Production, Energies, 11 (2018), pp. 156. doi.org/10.3390/en11010156
  74. Tam, P.E., Coxsackievirus myocarditis: interplay between virus and host in the pathogenesis of heart disease, Viral immunology, 19 (2006), 2, pp. 133-146
  75. Wang, Q., et al., Molecular basis of differential receptor usage for naturally occurring CD55-binding and -nonbinding coxsackievirus B3 strains, Proceedings of the National Academy of Sciences of the United States of America, 119 (2022), 4, pp. e2118590119
  76. ***, National Center for Biotechnology Information, www.ncbi.nlm.nih.gov/
  77. Sayers, E. W., et al., Database resources of the national center for biotechnology information, Nucleic Acids Research, 50 (2022), D1, pp. D20-D26
  78. Armstrong, D.R., et al., PDBe: improved findability of macromolecular structure data in the PDB, Nucleic Acids Research, 48 (2020), D1, pp. D335-D343
  79. ***, PDBe database, www.ebi.ac.uk/pdbe/
  80. PDBe-KB consortium, PDBe-KB: a community-driven resource for structural and functional annotations, Nucleic acids research, 48 (2020), D1, pp. D344-D353
  81. wwPDB consortium, Protein Data Bank: the single global archive for 3D macromolecular structure data, Nucleic acids research, 47 (2019), D1, pp. D520-D528
  82. Berman, H., et al., Announcing the worldwide Protein Data Bank, Nature structural biology, 10 (2003), 12, pp. 980
  83. Muckelbauer, J. K., et al., The structure of coxsackievirus B3 at 3.5 A resolution, Structure, 3 (1995), 7, pp. 653-667
  84. ***, UniProt database, www.uniprot.org/uniprotkb/G3KG26/entry
  85. Goodfellow, I. G., et al., Inhibition of coxsackie B virus infection by soluble forms of its receptors: binding affinities, altered particle formation, and competition with cellular receptors, Journal of Virology, 79 (2005), 18, pp. 12016-12024
  86. Shakeel, S., et al., Structural and functional analysis of coxsackievirus A9 integrin αvβ6 binding and uncoating, Journal of Virology, 87 (2013), 7, pp. 3943-3951
  87. Cui, Y., et al., Molecular basis of Coxsackievirus A10 entry using the two-in-one attachment and uncoating receptor KRM1, Proceedings of the National Academy of Sciences of the United States of America, 117 (2020), 31, pp. 18711-18718
  88. ***, NCBI database, www.ncbi.nlm.nih.gov/nuccore/KR815992.1/
  89. ***, NCBI database, www.ncbi.nlm.nih.gov/nuccore/D00627.1
  90. ***, NCBI database, www.ncbi.nlm.nih.gov/nuccore/MH118035.1
  91. ***, NCBI database, www.ncbi.nlm.nih.gov/nuccore/JN228097.1
  92. ***, NCBI database, www.ncbi.nlm.nih.gov/nuccore/NC_038307.1
  93. ***, NCBI database, www.ncbi.nlm.nih.gov/nuccore/DQ480420.1
  94. ***, PDBe database, www.ebi.ac.uk/pdbe/entry/pdb/7qw9
  95. Büttner, C.R., et al., Cryo-electron microscopy and image classification reveal the existence and structure of the coxsackievirus A6 virion, Communications biology, 5 (2022), 1, pp. 898
  96. ***, PDBe database, www.ebi.ac.uk/pdbe/entry/pdb/8at5
  97. Domanska, A., et al., Structural Studies Reveal that Endosomal Cations Promote Formation of Infectious Coxsackievirus A9 A-Particles, Facilitating RNA and VP4 Release, Journal of Virology, 96 (2022), 24, pp. e0136722
  98. ***, PDBe database, www.ebi.ac.uk/pdbe/entry/pdb/6smg
  99. Zhao, Y., et al., Hand-foot-and-mouth disease virus receptor KREMEN1 binds the canyon of Coxsackie Virus A10, Nature communications, 11 (2020), 1, pp. 38
  100. ***, PDBe database, www.ebi.ac.uk/pdbe/entry/pdb/4q4x
  101. Zocher, G., et al., A sialic acid binding site in a human picornavirus, PLoS pathogens, 10 (2014), 10, pp. e1004401
  102. ***, PDBe database, www.ebi.ac.uk/pdbe/entry/pdb/7vxh
  103. ***, NCBI database, www.ncbi.nlm.nih.gov/protein/AAB22445.2/
  104. ***, NCBI database, www.ncbi.nlm.nih.gov/protein/AAB22446.1
  105. ***, NCBI database, www.ncbi.nlm.nih.gov/protein/6ZCK_C
  106. ***, NCBI database, www.ncbi.nlm.nih.gov/protein/BAE06045.1
  107. 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), pp. 107621
  108. 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), pp. 2051-2067
  109. Thornton, W. M., XV. The relation of oxygen to the heat of combustion of organic compounds, The London, Edinburgh, and Dublin Philosophical Magazine and Journal of Science, 33 (1917), 194, pp. 196-203
  110. Atkins, P. W., de Paula, J., Physical Chemistry for the Life Sciences (2nd edition), W. H. Freeman and Company, New York, USA, 2011
  111. Riedel, S., et al., Jawetz, Melnick and Adelberg's Medical Microbiology, 28th ed., McGraw-Hill, New York, USA, 2019
  112. Seitsonen, J. J., et al., Structural analysis of coxsackievirus A7 reveals conformational changes associated with uncoating, Journal of Virology, 86 (2012), 13, pp. 7207-7215
  113. Ma, E., et al., Estimation of the basic reproduction number of enterovirus 71 and coxsackievirus A16 in hand, foot, and mouth disease outbreaks, The Pediatric infectious disease journal, 30 (2011), 8, pp. 675-679
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The silent assassin: Empirical formulas, molar masses, biosynthesis reactions, enthalpies, entropies and Gibbs energies of biosynthesis and Gibbs energies of binding of Coxsackieviruses A and B