Extracellular ionic fluxes suggest the basis for cellular life at the 1/f ridge of extended criticality

ABSTRACT: The criticality hypothesis states that a system may be poised in a critical state at the boundary between different types of dynamics. Previous studies have suggested that criticality has been evolutionarily selected, and examples have been found in cortical cell cultures and in the human nervous system. However, no one has yet reported a single- or multi-cell ensemble that was investigated ex vivo and found to be in the critical state. Here, the precise 1/f noise was found for pollen tube cells of optimum growth and for the physiological (“healthy”) state of blood cells. We show that the multi-scale processes that arise from the so-called critical phenomena can be a fundamental property of a living cell. Our results reveal that cell life is conducted at the border between order and disorder, and that the dynamics themselves drive a system towards a critical state. Moreover, a temperature-driven re-entrant state transition, manifest in the form of a Lorentz resonance, was found in the fluctuation amplitude of the extracellular ionic fluxes for the ensemble of elongating pollen tubes of Nicotiana tabacum L. or Hyacintus orientalis L. Since this system is fine-tuned for rapid expansion to reach the ovule at a critical temperature which results in fertilisation, the core nature of criticality (long-range coherence) offers an explanation for its potential in cell growth. We suggest that the autonomous organisation of expansive growth is accomplished by self-organised criticality, which is an orchestrated instability that occurs in an evolving cell. GRAPHIC ABSTRACT: [Image: see text] ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1007/s00249-020-01430-3) contains supplementary material, which is available to authorized users.