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Metabolic scaling in small life forms

Published 16 Dec 2023 in physics.bio-ph | (2403.00001v1)

Abstract: Metabolic scaling is one of the most important patterns in biology. Theory explaining the 3/4-power size-scaling of biological metabolic rate does not predict the non-linear scaling observed for smaller life forms. Here we present a new model for cells $<10{-8}$ m${3}$ that maximizes power from the reaction-displacement dynamics of enzyme-catalyzed reactions. Maximum metabolic rate is achieved through an allocation of cell volume to optimize a ratio of reaction velocity to molecular movement. Small cells $< 10{-17}$ m${3}$ generate power under diffusion by diluting enzyme concentration as cell volume increases. Larger cells require bulk flow of cytoplasm generated by molecular motors. These outcomes predict curves with literature-reported parameters that match the observed scaling of metabolic rates for unicells, and predicts the volume at which Prokaryotes transition to Eukaryotes. We thus reveal multiple size-dependent physical constraints for microbes in a model that extends prior work to provide a parsimonious hypothesis for how metabolism scales across small life.

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References (56)
  1. J. H. Brown, J. F. Gillooly, A. P. Allen, V. M. Savage, and G. B. West, “Toward a metabolic theory of ecology,” Ecology, vol. 85, no. 7, pp. 1771–1789, 2004.
  2. B. Enquist et al., “Scaling metabolism from organisms to ecosystems,” Nature, vol. 423, pp. 639–642, 2003.
  3. M. Kaspari, “Using the metabolic theory of ecology to predict global patterns of abundance,” Ecology, vol. 85, no. 7, pp. 1800–1802, 2004.
  4. Princeton: Princeton University, 2009.
  5. S. Pawar, A. Dell, and V. Savage, “Dimensionality of consumer search space drives trophic interaction strengths,” Nature, vol. 486, pp. 485–489, 2012.
  6. P. Agutter and J. Tuszynski, “Analytic theories of allometric scaling,” Journal of Experimental Biology, vol. 214, no. 7, pp. 1055–1062, 2011.
  7. D. Glazier, “A unifying explanation for diverse metabolic scaling in animals and plants,” Biological Reviews, vol. 85, pp. 111–138, 2010.
  8. K. Schmidt-Nielsen, Scaling: why is animal size so important? Cambridge UK: Cambridge University Press, 1984.
  9. R. Peters, The ecological implications of body size. Cambridge UK: Cambridge University Press, 1986.
  10. G. B. West, J. H. Brown, and B. J. Enquist, “A general model for the origin of allometric scaling laws in biology,” Science, vol. 276, no. 5309, pp. 122–126, 1997.
  11. G. B. West, J. H. Brown, and B. J. Enquist, “A general model for the structure and allometry of plant vascular systems,” Nature, vol. 400, no. 6745, pp. 664–667, 1999.
  12. S. Mori, K. Yamaji, A. Ishida, S. G. Prokushkin, O. V. Masyagina, A. Hagihara, A. R. Hoque, R. Suwa, A. Osawa, T. Nishizono, et al., “Mixed-power scaling of whole-plant respiration from seedlings to giant trees,” Proceedings of the National Academy of Sciences, vol. 107, no. 4, pp. 1447–1451, 2010.
  13. J. R. Banavar, J. Damuth, A. Maritan, and A. Rinaldo, “Supply–demand balance and metabolic scaling,” Proceedings of the National Academy of Sciences, vol. 99, no. 16, pp. 10506–10509, 2002.
  14. J. Banavar et al., “A general basis for quarter-power scaling in animals,” Proceedings of the National Academy of Sciences, vol. 107, pp. 15816–15820, 2010.
  15. J. Maino, M. Kearney, R. Nisbet, and S. Kooijman, “Reconciling theories for metabolic scaling,” Journal of Animal Ecology, vol. 83, pp. 20–29, 2014.
  16. J. P. DeLong, J. G. Okie, M. E. Moses, R. M. Sibly, and J. H. Brown, “Shifts in metabolic scaling, production, and efficiency across major evolutionary transitions of life,” Proceedings of the National Academy of Sciences, vol. 107, no. 29, pp. 12941–12945, 2010.
  17. D. Glazier, “Metabolic scaling in complex living systems,” Systems, vol. 2, no. 4, p. 451, 2014.
  18. T. Kolokotrones, V. Savage, E. Deeds, and W. Fontana, “Curvature in metabolic scaling,” Nature, vol. 464, no. 7289, pp. 753–756, 2010.
  19. G. West and J. Brown, “The origin of allometric scaling laws in biology from genomes to ecosystems: towards a quantitative unifying theory of biological structure and organization,” Journal of Experimental Biology, vol. 208, pp. 1575–1592, 2005.
  20. A. Makarieva et al., “Mean mass-specific metabolic rates are strikingly similar across life’s major domains: Evidence for life’s metabolic optimum,” Proceedings of the National Academy of Sciences, vol. 105, pp. 16994–16999, 2008.
  21. C. P. Kempes, S. Dutkiewicz, and M. J. Follows, “Growth, metabolic partitioning, and the size of microorganisms,” Proceedings of the National Academy of Sciences, vol. 109, no. 2, pp. 495–500, 2012.
  22. C. P. Kempes, L. Wang, J. P. Amend, J. Doyle, and T. Hoehler, “Evolutionary tradeoffs in cellular composition across diverse bacteria,” The ISME journal, vol. 10, no. 9, pp. 2145–2157, 2016.
  23. C. P. Kempes, M. Koehl, and G. B. West, “The scales that limit: the physical boundaries of evolution,” Frontiers in Ecology and Evolution, vol. 7, p. 242, 2019.
  24. L. Demetrius, “Quantum statistics and allometric scaling of organisms,” Physica A: Statistical Mechanics and its Applications, vol. 322, pp. 477–490, 2003.
  25. D. S. Banks and C. Fradin, “Anomalous diffusion of proteins due to molecular crowding,” Biophysical journal, vol. 89, no. 5, pp. 2960–2971, 2005.
  26. F. Roosen-Runge, M. Hennig, F. Zhang, R. M. Jacobs, M. Sztucki, H. Schober, T. Seydel, and F. Schreiber, “Protein self-diffusion in crowded solutions,” Proceedings of the National Academy of Sciences, vol. 108, no. 29, pp. 11815–11820, 2011.
  27. A. Bar-Even, E. Noor, Y. Savir, W. Liebermeister, D. Davidi, D. S. Tawfik, and R. Milo, “The moderately efficient enzyme: evolutionary and physicochemical trends shaping enzyme parameters,” Biochemistry, vol. 50, no. 21, pp. 4402–4410, 2011.
  28. H. Schulz, T. Brinkhoff, T. G. Ferdelman, M. H. Mariné, A. Teske, and B. B. Jørgensen, “Dense populations of a giant sulfur bacterium in namibian shelf sediments,” Science, vol. 284, no. 5413, pp. 493–495, 1999.
  29. N. Lane and W. Martin, “The energetics of genome complexity,” Nature, vol. 467, no. 7318, pp. 929–934, 2010.
  30. J.-M. Volland, S. Gonzalez-Rizzo, O. Gros, T. Tyml, N. Ivanova, F. Schulz, D. Goudeau, N. H. Elisabeth, N. Nath, D. Udwary, et al., “A centimeter-long bacterium with dna contained in metabolically active, membrane-bound organelles,” Science, vol. 376, no. 6600, pp. 1453–1458, 2022.
  31. K. Luby-Phelps, “Cytoarchitecture and physical properties of cytoplasm: volume, viscosity, diffusion, intracellular surface area,” International review of cytology, vol. 192, pp. 189–221, 1999.
  32. S. M. Hurtley, “Cell biology of the cytoskeleton,” 1998.
  33. M. Xu, J. L. Ross, L. Valdez, and A. Sen, “Direct single molecule imaging of enhanced enzyme diffusion,” Physical review letters, vol. 123, no. 12, p. 128101, 2019.
  34. N. Fakhri, A. D. Wessel, C. Willms, M. Pasquali, D. R. Klopfenstein, F. C. MacKintosh, and C. F. Schmidt, “High-resolution mapping of intracellular fluctuations using carbon nanotubes,” Science, vol. 344, no. 6187, pp. 1031–1035, 2014.
  35. C. P. Brangwynne, G. H. Koenderink, F. C. MacKintosh, and D. A. Weitz, “Intracellular transport by active diffusion,” Trends in cell biology, vol. 19, no. 9, pp. 423–427, 2009.
  36. P. C. Bressloff and J. M. Newby, “Stochastic models of intracellular transport,” Reviews of Modern Physics, vol. 85, no. 1, p. 135, 2013.
  37. S. S. Mogre, A. I. Brown, and E. F. Koslover, “Getting around the cell: physical transport in the intracellular world,” Physical Biology, vol. 17, no. 6, p. 061003, 2020.
  38. Z. Qu, D. Schildknecht, S. Shadkhoo, E. Amaya, J. Jiang, H. J. Lee, D. Larios, F. Yang, R. Phillips, and M. Thomson, “Persistent fluid flows defined by active matter boundaries,” Communications Physics, vol. 4, no. 1, p. 198, 2021.
  39. M. J. Bowick, N. Fakhri, M. C. Marchetti, and S. Ramaswamy, “Symmetry, thermodynamics, and topology in active matter,” Physical Review X, vol. 12, no. 1, p. 010501, 2022.
  40. M. Guo, A. J. Ehrlicher, M. H. Jensen, M. Renz, J. R. Moore, R. D. Goldman, J. Lippincott-Schwartz, F. C. Mackintosh, and D. A. Weitz, “Probing the stochastic, motor-driven properties of the cytoplasm using force spectrum microscopy,” Cell, vol. 158, no. 4, pp. 822–832, 2014.
  41. R. Lipowsky, S. Klumpp, and T. M. Nieuwenhuizen, “Random walks of cytoskeletal motors in open and closed compartments,” Physical Review Letters, vol. 87, no. 10, p. 108101, 2001.
  42. P. Pierobon, M. Mobilia, R. Kouyos, and E. Frey, “Bottleneck-induced transitions in a minimal model for intracellular transport,” Physical Review E, vol. 74, no. 3, p. 031906, 2006.
  43. BioRender.com, “Created with biorender.com.”
  44. B. Trickovic and M. Lynch, “Resource allocation to cell envelopes and the scaling of bacterial growth rate,” BioRxiv, pp. 2022–01, 2022.
  45. M. Lynch and G. K. Marinov, “The bioenergetic costs of a gene,” Proceedings of the National Academy of Sciences, vol. 112, no. 51, pp. 15690–15695, 2015.
  46. S. Alberti, “Phase separation in biology,” Current Biology, vol. 27, no. 20, pp. R1097–R1102, 2017.
  47. C. A. Azaldegui, A. G. Vecchiarelli, and J. S. Biteen, “The emergence of phase separation as an organizing principle in bacteria,” Biophysical journal, vol. 120, no. 7, pp. 1123–1138, 2021.
  48. D. Zwicker, “The intertwined physics of active chemical reactions and phase separation,” Current Opinion in Colloid & Interface Science, p. 101606, 2022.
  49. M. Castellana, S. Hsin-Jung Li, and N. S. Wingreen, “Spatial organization of bacterial transcription and translation,” Proceedings of the National Academy of Sciences, vol. 113, no. 33, pp. 9286–9291, 2016.
  50. N. S. Wingreen and K. C. Huang, “Physics of intracellular organization in bacteria,” Annual Review of Microbiology, vol. 69, pp. 361–379, 2015.
  51. G. B. West, J. H. Brown, and B. J. Enquist, “The fourth dimension of life: fractal geometry and allometric scaling of organisms,” science, vol. 284, no. 5420, pp. 1677–1679, 1999.
  52. V. M. Savage, L. P. Bentley, B. J. Enquist, J. S. Sperry, D. Smith, P. B. Reich, and E. Von Allmen, “Hydraulic trade-offs and space filling enable better predictions of vascular structure and function in plants,” Proceedings of the National Academy of Sciences, vol. 107, no. 52, pp. 22722–22727, 2010.
  53. A. B. Brummer, V. M. Savage, and B. J. Enquist, “A general model for metabolic scaling in self-similar asymmetric networks,” PLoS computational biology, vol. 13, no. 3, p. e1005394, 2017.
  54. T. Rodrigues-Oliveira, F. Wollweber, R. I. Ponce-Toledo, J. Xu, S. K.-M. Rittmann, A. Klingl, M. Pilhofer, and C. Schleper, “Actin cytoskeleton and complex cell architecture in an asgard archaeon,” Nature, vol. 613, no. 7943, pp. 332–339, 2023.
  55. B. Avcı, J. Brandt, D. Nachmias, N. Elia, M. Albertsen, T. J. Ettema, A. Schramm, and K. U. Kjeldsen, “Spatial separation of ribosomes and dna in asgard archaeal cells,” The ISME Journal, vol. 16, no. 2, pp. 606–610, 2022.
  56. H. Imachi, M. K. Nobu, N. Nakahara, Y. Morono, M. Ogawara, Y. Takaki, Y. Takano, K. Uematsu, T. Ikuta, M. Ito, et al., “Isolation of an archaeon at the prokaryote–eukaryote interface,” Nature, vol. 577, no. 7791, pp. 519–525, 2020.

Summary

  • The paper presents a novel model that links thermodynamics with reaction-diffusion dynamics to explain non-linear metabolic scaling in small cells.
  • It accurately replicates the metabolic rate transition from prokaryotes to eukaryotes by predicting the cell volume threshold for evolutionary shifts.
  • The derived scaling relation (B = B₀ Vc^(11/15)) and enzyme dilution insights offer key implications for optimizing cellular metabolism and understanding evolutionary trade-offs.

Insights on Metabolic Scaling in Small Life Forms

The paper, Metabolic scaling in small life forms by Mark E. Ritchie and Christopher P. Kempes, explores the intricacies of metabolic scaling within unicellular organisms and elucidates the discrepancies between traditional theories and observed data in microbial systems. Given the established 3/4-power scaling rule for larger life forms, which articulates how metabolic rates scale with body mass, this research ambitiously extends into the microdomain, offering a novel perspective on the scaling patterns of smaller-sized life forms. The essence of this study lies in addressing the non-linear scaling observed in smaller organisms, which diverges from the anticipations of the 3/4-power law.

The authors propose a comprehensive model integrating thermodynamic principles with reaction-diffusion dynamics to elucidate metabolic scaling mechanisms across a vast range of cell sizes. This model highlights the significance of optimizing the allocation of cell volume to achieve maximal metabolic power. Specifically, for cells with volume less than 101710^{-17} m3^3, power is generated under diffusion by strategically diluting enzyme concentration as the cell volume increases. As the cell size grows, the metabolic processes transition to necessitating bulk flow facilitated by molecular motors, marking a distinct shift in the mechanism driving metabolic rates.

A notable achievement of this model is its ability to replicate and explain the observed transitions between prokaryotes and eukaryotes based on size-dependent constraints. This model significantly enhances our understanding by predicting the volume transition threshold where prokaryotes evolve into eukaryotes, a fundamentally important point in evolutionary biology. Such predictions are substantiated through extensive parameterization with existing literature, ensuring alignment with empirical data concerning the metabolic rates of unicellular organisms.

A profound implication of these findings is the guidance they provide for hypotheses concerning the evolutionary trajectories of microbial life. By elucidating the underpinning physical and chemical constraints that govern metabolic scaling, this paper paves the way for more accurate models that can improve predictive capabilities related to growth rates and ribosomal abundance, contributing largely to the understanding of evolutionary trade-offs.

An essential output of this study is the derivation of a scaling relation B=B0Vc11/15B = B_0 V_c^{11/15}, offering a refined alternative to previous models and aligning closely with empirical data. The model also uncovers the substrate-enzyme dynamic, suggesting that the optimal concentration of enzymes should scale with cell size in a manner that minimizes diffusion constraints while maximizing reaction efficiency. Such insights expose the critical trade-offs between cellular transport mechanisms and metabolic energy constraints, presenting potential avenues for future research into the evolving complexity of cellular life.

In summary, the paper significantly advances the understanding of metabolic scaling in microscopic life forms by providing a robust theoretical framework that captures the observed deviations from traditional scaling laws within these size domains. This model is instrumental for future research, potentially extending into more complex analyses that incorporate additional biological constraints and evolutionary factors. The model’s versatility in predicting metabolic rates across various cellular sizes, along with its conformance to empirical data, highlights its relevance and potential for widespread application within biological and ecological sciences.

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