The Unconventionality of Nature: Biology, from Noise to Functional Randomness

In biology, phenotypes’ variability stems from stochastic gene expression as well as from extrinsic fluctuations that are largely based on the contingency of developmental paths and on ecosystemic changes. Both forms of randomness constructively contribute to biological robustness, as resilience, far away from conventional computable dynamics, where elaboration and transmission of information are robust when they resist to noise. We first survey how fluctuations may be inserted in biochemical equations as probabilistic terms, in conjunction to diffusion or path integrals, and treated by statistical approaches to physics. Further work allows to better grasp the role of biological “resonance” (interactions between different levels of organization) and plasticity, in a highly unconventional frame that seems more suitable for biological processes. In contrast to physical conservation properties, thus symmetries, symmetry breaking is particularly relevant in biology; it provides another key component of biological historicity and of randomness as a source of diversity and, thus, of onto-phylogenetic stability and organization as these are also based on variation and adaptativity.

[1]  M. Delbrück The Burst Size Distribution in the Growth of Bacterial Viruses (Bacteriophages) , 1945, Journal of bacteriology.

[2]  E. O’Shea,et al.  Living with noisy genes: how cells function reliably with inherent variability in gene expression. , 2007, Annual review of biophysics and biomolecular structure.

[3]  J. Elf,et al.  Fast evaluation of fluctuations in biochemical networks with the linear noise approximation. , 2003, Genome research.

[4]  Angelo Vulpiani,et al.  Chaos and Coarse Graining in Statistical Mechanics , 2008 .

[5]  Marco Buiatti,et al.  Towards a statistical characterisation of the living state of matter , 2004 .

[6]  C. Sonnenschein,et al.  Environmental causes of cancer: endocrine disruptors as carcinogens , 2010, Nature Reviews Endocrinology.

[7]  Gerhard Werner,et al.  Metastability, criticality and phase transitions in brain and its models , 2007, Biosyst..

[8]  E. Braun,et al.  Collective Dynamics of Gene Expression in Cell Populations , 2011, PloS one.

[9]  Ulrich Weiss,et al.  MACROSCOPIC QUANTUM COHERENCE , 1986 .

[10]  Francis Bailly,et al.  BIOLOGICAL ORGANIZATION AND ANTI-ENTROPY , 2009 .

[11]  C. Rao,et al.  Control, exploitation and tolerance of intracellular noise , 2002, Nature.

[12]  G. Longo,et al.  Randomness and Multi-level Interactions in Biology , 2011 .

[13]  A. Lesne Robustness: confronting lessons from physics and biology , 2008, Biological reviews of the Cambridge Philosophical Society.

[14]  A. Roeder,et al.  Stochasticity in plant cellular growth and patterning , 2014, Front. Plant Sci..

[15]  Cristian S. Calude,et al.  Strong Kochen-Specker theorem and incomputability of quantum randomness , 2012, Physical Review A.

[16]  N. Kampen,et al.  Stochastic processes in physics and chemistry , 1981 .

[17]  M. Bizzarri,et al.  Gravity sensing by cells: mechanisms and theoretical grounds , 2014, Rendiconti Lincei.

[18]  Austin G Smith,et al.  The ground state of pluripotency. , 2010, Biochemical Society transactions.

[19]  E. Allin,et al.  Evolution of the mammalian middle ear , 1975, Journal of morphology.

[20]  Vincent Fleury,et al.  Coupling of Growth, Differentiation and Morphogenesis: An Integrated Approach to Design in Embryogenesis , 2012 .

[21]  R. Feynman,et al.  Space-Time Approach to Non-Relativistic Quantum Mechanics , 1948 .

[22]  Giuliano Preparata,et al.  A new QED picture of water: Understanding a few fascinating phenomena , 1998 .

[23]  B. Snijder,et al.  Origins of regulated cell-to-cell variability , 2011, Nature Reviews Molecular Cell Biology.

[24]  Yu-Pin Luo,et al.  Fluctuations in gene regulatory networks as Gaussian colored noise. , 2009, The Journal of chemical physics.

[25]  J. Elgin The Fokker-Planck Equation: Methods of Solution and Applications , 1984 .

[26]  S. Jay Olshansky,et al.  At the Heart of Aging: is it Metabolic Rate or Stability? , 2005, Biogerontology.

[27]  D. Wilkinson Stochastic modelling for quantitative description of heterogeneous biological systems , 2009, Nature Reviews Genetics.

[28]  M. Khammash,et al.  STOCHASTIC MODELING OF THE PAP PILI EPIGENETIC SWITCH , 2005 .

[29]  D. Gillespie A General Method for Numerically Simulating the Stochastic Time Evolution of Coupled Chemical Reactions , 1976 .

[30]  Cristian S. Calude,et al.  Classical, quantum and biological randomness as relative unpredictability , 2015, Natural Computing.

[31]  J. Sethna Statistical Mechanics: Entropy, Order Parameters, and Complexity , 2021 .

[32]  S. Gould,et al.  Punctuated equilibria: an alternative to phyletic gradualism , 1972 .

[33]  Giuseppe Longo,et al.  Extended Criticality, Phase Spaces and Enablement in Biology , 2013 .

[34]  M. Ehrenberg,et al.  Stochastic focusing: fluctuation-enhanced sensitivity of intracellular regulation. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[35]  M. Delbrück Statistical Fluctuations in Autocatalytic Reactions , 1940 .

[36]  C. Sonnenschein,et al.  The society of cells cancer and control of cell proliferation , 2013 .

[37]  Marco Buiatti,et al.  Chance vs. necessity in living systems: a false antinomy. , 2008, Rivista di biologia.

[38]  David K. Karig,et al.  Noise in biological circuits. , 2009, Wiley interdisciplinary reviews. Nanomedicine and nanobiotechnology.

[39]  Benoit Landrein,et al.  Mechanical Stress Acts via Katanin to Amplify Differences in Growth Rate between Adjacent Cells in Arabidopsis , 2012, Cell.

[40]  M. Elowitz,et al.  Functional roles for noise in genetic circuits , 2010, Nature.

[41]  S. Leibler,et al.  Mechanisms of noise-resistance in genetic oscillators , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[42]  G. Roger,et al.  Experimental Test of Bell's Inequalities Using Time- Varying Analyzers , 1982 .

[43]  J. Hillston,et al.  Stochastic properties of the plant circadian clock , 2012, Journal of The Royal Society Interface.

[44]  François Taddei,et al.  Asymmetric segregation of protein aggregates is associated with cellular aging and rejuvenation , 2008, Proceedings of the National Academy of Sciences.

[45]  Johannes Berg,et al.  What makes the lac-pathway switch: identifying the fluctuations that trigger phenotype switching in gene regulatory systems , 2013, Nucleic acids research.

[46]  Julien F. Ollivier,et al.  Colored extrinsic fluctuations and stochastic gene expression , 2008, Molecular systems biology.

[47]  Giuseppe Longo,et al.  From Bottom-Up Approaches to Levels of Organization and Extended Critical Transitions , 2012, Front. Physio..

[48]  Paul-Antoine Miquel,et al.  Aging as alteration. , 2014, Interdisciplinary topics in gerontology.

[49]  G. Longo,et al.  Perspectives on Organisms , 2014, Lecture Notes in Morphogenesis.

[50]  Giuseppe Longo,et al.  Mathematical Structures in Computer Science , 2012 .

[51]  E. Schrödinger,et al.  What is life? : the physical aspect of the living cell , 1946 .

[52]  François Taddei,et al.  In Brief , 2003, Nature Reviews Microbiology.

[53]  Arezki Boudaoud,et al.  Noise and Robustness in Phyllotaxis , 2012, PLoS Comput. Biol..

[54]  A. Vulpiani,et al.  Reductionism, Emergence and Levels of Reality: The Importance of Being Borderline , 2014 .

[55]  Péter Gács,et al.  Randomness on Computable Probability Spaces—A Dynamical Point of View , 2009, Theory of Computing Systems.

[56]  G. Longo,et al.  In search of principles for a Theory of Organisms , 2015, Journal of Biosciences.

[57]  G. Longo,et al.  Perspectives on Organisms: Biological time, Symmetries and Singularities , 2014 .

[58]  François Taddei,et al.  Pre-dispositions and epigenetic inheritance in the Escherichia coli lactose operon bistable switch , 2010, Molecular systems biology.

[59]  Eytan Domany,et al.  Introduction to the renormalization group and to critical phenomena , 1977 .

[60]  W. Bialek,et al.  Are Biological Systems Poised at Criticality? , 2010, 1012.2242.

[61]  Jeffrey W. Smith,et al.  Stochastic Gene Expression in a Single Cell , .

[62]  Upinder S Bhalla,et al.  Understanding complex signaling networks through models and metaphors. , 2003, Progress in biophysics and molecular biology.

[63]  M. Buiatti,et al.  Plants: Individuals or Epigenetic Cell Populations? , 2011 .

[64]  Albert Libchaber,et al.  Universal protein fluctuations in populations of microorganisms. , 2012, Physical review letters.

[65]  Giuseppe Longo,et al.  Randomness and multilevel interactions in biology , 2011, Theory in Biosciences.

[66]  P. Swain,et al.  Intrinsic and extrinsic contributions to stochasticity in gene expression , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[67]  A. Arkin,et al.  Stochastic kinetic analysis of developmental pathway bifurcation in phage lambda-infected Escherichia coli cells. , 1998, Genetics.

[68]  H. Kleinert Path Integrals in Quantum Mechanics, Statistics, Polymer Physics, and Financial Markets , 2006 .

[69]  L. Landweber,et al.  Epigenetic inheritance in ciliates. , 2009, Current opinion in microbiology.

[70]  Emmanuel Farge L'embryon sous l'emprise des gènes et de la pression , 2009 .

[71]  A. M. Turing,et al.  The chemical basis of morphogenesis , 1952, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences.

[72]  R. Rohwer Order out of Chaos: Man's New Dialogue with Nature , 1986 .

[73]  Giuseppe Longo,et al.  No entailing laws, but enablement in the evolution of the biosphere , 2012, GECCO '12.

[74]  S. Leibler,et al.  Robustness in simple biochemical networks , 1997, Nature.

[75]  M. Mossio,et al.  Biological organisation as closure of constraints. , 2015, Journal of theoretical biology.

[76]  A. Oudenaarden,et al.  Nature, Nurture, or Chance: Stochastic Gene Expression and Its Consequences , 2008, Cell.

[77]  M Matsuo,et al.  [Oxidative stress and aging]. , 1997, Nihon Ronen Igakkai zasshi. Japanese journal of geriatrics.

[78]  David Klatzmann,et al.  Comprehensive Assessment and Mathematical Modeling of T Cell Population Dynamics and Homeostasis1 , 2008, The Journal of Immunology.

[79]  J. Monod Le hasard et la nécessité , 1970 .

[80]  Robert Zwanzig,et al.  Memory Effects in Irreversible Thermodynamics , 1961 .

[81]  Cristian S. Calude,et al.  Classical , Quantum and Biological Randomness as Relative Incomputability , 2014 .