Bio-analog dissipative structures and principles of biological behavior.

The place of living organisms in the natural world is a nearly perennial question in philosophy and the sciences; how can inanimate matter yield animate beings? A dominant answer for several centuries has been to treat organisms as sophisticated machines, studying them with the mechanistic physics and chemistry that have given rise to technology and complex machines. Since the early 20th century, many scholars have sought instead to naturalize biology through thermodynamics, recognizing the precarious far-from-equilibrium state of organisms. Erwin Bauer was an early progenitor of this perspective with ambitions of "general laws for the movement of living matter". In addition to taking a thermodynamic perspective, Bauer recognized that organisms are fundamentally behaving systems, and that explaining the physics of life requires explaining the origins of intentionality, adaptability, and self-regulation. Bauer, like some later scholars, seems to advocate for a "new physics", one that extends beyond mechanics and classical thermodynamic, one that would be inclusive of living systems. In this historical review piece, we explore some of Bauer's ideas and explain how similar concepts have been explored in modern non-equilibrium thermodynamics and dissipative structure theory. Non-living dissipative structures display end-directedness, self-maintenance, and adaptability analogous to organisms. These findings also point to an alternative framework for the life sciences, that treats organisms not as machines but as sophisticated dissipative structures. We evaluate the differences between mechanistic and thermodynamic perspectives on life, and what each theory entails for understanding the behavior of organisms.

Foraging Dynamics and Entropy Production in a Simulated Proto-Cell.

All organisms depend on a supply of energetic resources to power behavior and the irreversible entropy-producing processes that sustain them. Dissipative structure theory has often been a source of inspiration for better understanding the thermodynamics of biology, yet real organisms are inordinately more complex than most laboratory systems. Here we report on a simulated chemical dissipative structure that operates as a proto cell. The simulated swimmer moves through a 1D environment collecting resources that drive a nonlinear reaction network interior to the swimmer. The model minimally represents properties of a simple organism including rudimentary foraging and chemotaxis and an analog of a metabolism in the nonlinear reaction network. We evaluated how dynamical stability of the foraging dynamics (i.e., swimming and chemotaxis) relates to the rate of entropy production. Results suggested a relationship between dynamical steady states and entropy production that was tuned by the relative coordination of foraging and metabolic processes. Results include evidence in support of and contradicting one formulation of a maximum entropy production principle. We discuss the status of this principle and its relevance to biology.

Functional Interdependence in Coupled Dissipative Structures: Physical Foundations of Biological Coordination.

Coordination within and between organisms is one of the most complex abilities of living systems, requiring the concerted regulation of many physiological constituents, and this complexity can be particularly difficult to explain by appealing to physics. A valuable framework for understanding biological coordination is the coordinative structure, a self-organized assembly of physiological elements that collectively performs a specific function. Coordinative structures are characterized by three properties: (1) multiple coupled components, (2) soft-assembly, and (3) functional organization. Coordinative structures have been hypothesized to be specific instantiations of dissipative structures, non-equilibrium, self-organized, physical systems exhibiting complex pattern formation in structure and behaviors. We pursued this hypothesis by testing for these three properties of coordinative structures in an electrically-driven dissipative structure. Our system demonstrates dynamic reorganization in response to functional perturbation, a behavior of coordinative structures called reciprocal compensation. Reciprocal compensation is corroborated by a dynamical systems model of the underlying physics. This coordinated activity of the system appears to derive from the system's intrinsic end-directed behavior to maximize the rate of entropy production. The paper includes three primary components: (1) empirical data on emergent coordinated phenomena in a physical system, (2) computational simulations of this physical system, and (3) theoretical evaluation of the empirical and simulated results in the context of physics and the life sciences. This study reveals similarities between an electrically-driven dissipative structure that exhibits end-directed behavior and the goal-oriented behaviors of more complex living systems.

Dissipative Structures, Organisms and Evolution.

Self-organization in nonequilibrium systems has been known for over 50 years. Under nonequilibrium conditions, the state of a system can become unstable and a transition to an organized structure can occur. Such structures include oscillating chemical reactions and spatiotemporal patterns in chemical and other systems. Because entropy and free-energy dissipating irreversible processes generate and maintain these structures, these have been called dissipative structures. Our recent research revealed that some of these structures exhibit organism-like behavior, reinforcing the earlier expectation that the study of dissipative structures will provide insights into the nature of organisms and their origin. In this article, we summarize our study of organism-like behavior in electrically and chemically driven systems. The highly complex behavior of these systems shows the time evolution to states of higher entropy production. Using these systems as an example, we present some concepts that give us an understanding of biological organisms and their evolution.

Particle Flock Motion at Air-Water Interface Driven by Interfacial Free Energy Foraging.

From flocks of birds and sheep to colonies of bacteria, complex patterns and self-motion are found in all hierarchies of nature. Artificial nonliving systems provide useful insight, since living systems are complicated and may involve cognitive issues not found in nonliving matter. Herein, we report naturally flocking irregularly shaped benzoquinone (BQ) particles on the air-water interface that cross a gate. In this open system designed with absence of external control, the particle flock moves by Marangoni "surfing" driven by slow dissolution of weakly surface active BQ postulated to create inhomogeneous interfacial tension fields. The particle flocks move collectively through a gate placed in the air-water interface to the side that has higher interfacial tension. Position-sensitive surface tension measurements used for the first time in a multiparticle Marangoni motion system show unequivocally that flock motion and gate crossing proceed to areas of slightly higher interfacial tension. Flock crossing is accompanied by a low-high differential interfacial tension change from one side of the gate to the other, with the flock moving to the side with higher interfacial tension. Thus, the flocks move because they are foraging for interfacial free energy.

Thermal- and Magnetic-Sensitive Particle Flocking Motion at the Air-Water Interface.

Collective self-motion of particulate systems provides novel opportunities for developing flocking and sensing functions from seemingly inanimate objects. In this paper, we report videos documenting spontaneous collective flocking of multiple irregularly shaped macroscopic benzoquinone (BQ) particles at the air-water interface. Self-propulsion occurs due to the Gibbs-Marangoni effect surface tension gradients generated by the BQ particles. The air-water interface develops inhomogeneous interfacial tension fields created by differential dissolution at points and edges of BQ particles, causing interfacial tension variations along the solid-liquid-air interfaces. Responses of irregularly shaped BQ particles to these driving forces do not result in random motion but lead to a cooperative hydrodynamic flocking. Curiously, the flocking behavior was very evident for irregularly shaped particles but not observed for symmetric circular BQ disks. The flock responds to changes in its local environment as it forages for interfacial free energy. It exhibits warm and cool thermotaxis and thus can sense local temperature changes. Also, though a single magnetic bead is not confined to a part of the Petri dish by an applied magnetic field, when this magnetic bead is a member of a flock in which all of the other beads are not magnetic, the flock as a whole moves and hovers around the region where the field is maximum. In other words, the magnetic bead becomes a kind of "sensor" for the flock to respond to a magnetic field, the response being a drift in the direction of the field.

Co-operative motion of multiple benzoquinone disks at the air-water interface.

Self-motion of physical-chemical systems is a promising avenue for studying and developing mechanical functions with inanimate systems. In this paper, we investigate spontaneous motion of collections of solid macroscopic benzoquinone (BQ) disks at the air-water interface without intervention of chemical reactions. The BQ particles slowly dissolve and create heterogeneous interfacial tension fields on the water surface that drive the motion. Spontaneous, continuous locomotion was observed between multiple BQ particles, along with coupling, collisions, cycling and collective foraging for interfacial free energy. Analysis of the motion suggests co-operative behavior depends strongly on particle shape.

Analysis of the mechanism of asymmetric amplification by chiral auxiliary trans-1,2-diaminocyclohexane bistriflamide.

Asymmetric amplification is a phenomenon in which the enantiomeric excess (ee) of a product is higher than that of a chiral auxiliary for a catalyst. We analyzed the mechanism of asymmetric amplification observed in the addition of diethylzinc (Et(2)Zn) to benzaldehyde (PhCHO) to synthesize 1-phenyl-1-propanol in the presence of trans-1,2-diaminocyclohexane bistriflamide (DCBF) and titanium tetraisopropoxide (TIOP). In a manner similar to the reaction in which 1-piperidino-3,3-dimethyl-2-butanol is a chiral auxiliary for the catalyst, when asymmetric amplification was observed, the ee of the product varied as the reaction progressed. The mechanisms of variation in ee in the two reactions, however, were different. No asymmetric amplification was observed when TIOP and PhCHO were added to a mixture of DCBF and Et(2)Zn, while the ee of the product was always higher than that of DCBF when PhCHO and Et(2)Zn were added to a mixture of DCBF and TIOP. In the latter case, the product ee decreased as the reaction progressed. The results indicate that DCBF forms inactive heterochiral complex causing an increase in the ee of DCBF in the solution, which is the chiral auxiliary for the catalyst. But the complex is not very stable and gradually dissociates due to the reaction with Et(2)Zn. As a result, the asymmetric amplification decreases as the reaction progresses.

Emergence of homochirality in far-from-equilibrium systems: mechanisms and role in prebiotic chemistry.

Since the model proposed by Frank (Frank FC, Biochem Biophys Acta 1953;11:459-463), several alternative models have been developed to explain how an asymmetric non-racemic steady state can be reached by a chirally symmetric chemical reactive system. This paper explains how a stable non-racemic regime can be obtained as a symmetry breaking occurring in a far-from-equilibrium reactive system initiated with an initial imbalance. Departing from the variations around the original Frank's model that are commonly described in the literature, i.e. open-flow systems of direct autocatalytic reactions, we discuss recent developments emphasizing both an active recycling of components and an autocatalytic network of simple reactions. We will present our APED model as the most natural realization of such thermodynamic openness and non-equilibrium, of recycling and of network autocatalysis, each of these in prebiotic conditions. The different experimental and theoretical models in the literature will be classified according to mechanism. The place and role of such self-structured networks responsible for the presence of homochirality in the primitive Earth will be detailed.

Experimental evidence and theoretical analysis for the chiral symmetry breaking in the growth front of conglomerate crystal phase of 1,1'-binaphthyl.

Chirally asymmetric states, chemical oscillations, propagating chemical waves, and spatial patterns, are examples of far-from-equilibrium self-organization. We have found that the crystal growth front of 1,1(')-binaphthyl shows many of the characteristics of an open system in which chiral symmetry breaking has occurred. From its supercooled molten phase, 1,1(')-binaphthyl crystallizes as a conglomerate of R and S crystals when the temperature is above 145 degrees C. In addition, 1,1(')-binaphthyl in its molten phase is always racemic due to its high racemization rate. Under appropriate conditions, bimodal probability distribution of enantiomeric excess (ee) with maxima around 60% was observed. The ee was mass independent, indicating that the growth front maintains a constant ee. A kinetic model that theoretically analyzes the chiral symmetry breaking transition in the growth front of a conglomerate crystal phase was formulated. Computer simulation of the model reproduced not only the average but also the large variation of the ee observed in crystallization experiments.

Three-dimensional description of the spontaneous onset of homochirality on the surface of a conglomerate crystal phase.

The spontaneous emergence of homochirality in an initially racemic system can be obtained in far-from-equilibrium states. Traditional models do not take into account the influence of inhomogeneities, while they may be of great importance. What would happen when one configuration emerges at one position, and the opposite one at another position? We present a discrete three-dimensional model of conglomerate crystallization, based on 1,1'-binaphthyl crystallization experiments, that takes into account the position and environment of every single elementary growth subunit. Stochastic simulations were performed to predict the evolution of the crystallization process. It is shown that the traditional view of the symmetry breaking can then be extended. Fluctuations of the fixed points related to inhomogeneities are observed, and complex behavior, such as local instabilities, transient structures, and chaotic behavior, can emerge. Our modeling indicates that such complex phenomena could cause large fluctuation of the final enantiomeric excess that is observed experimentally in binaphthyl crystallization. The results presented in this article show the importance of inhomogeneities in understanding enantiomeric excess generated in crystallization and the inadequacy of the models based on the assumption of homogeneity.

Kinetic model for the chiral symmetry breaking transition in the growth front of a conglomerate crystal phase.

In its molten phase, 1,1'-binaphthyl is racemic due to its high racemization rate, but it can crystallize as a conglomerate of R and S crystals. Our experiments have indicated that, under some conditions, the crystal growth front of 1,1'-binaphthyl shows many of the characteristics of an open system in which chiral symmetry is broken; i.e., the growing solid phase becomes predominantly R or S. Here we present a kinetic model to explain the observed chiral symmetry breaking. The model is based on growth due to attachment of R or S growth units to a crystal surface in a supercooled melt. Chiral symmetry breaking occurs due to chirally autocatalytic formation of R or S growth units on the growth surface. Unlike the many models suggested and studied in the 1980s, there is no cross-inhibition between R- and S-enantiomer in the model presented here. In our model, asymmetric and symmetric steady-state solutions that do not intersect were found. Through linear stability analysis, the critical point, at which a symmetric solution becomes unstable and makes a transition to an asymmetric solution, is determined.

Chiral symmetry-breaking transition in growth front of crystal phase of 1,1'-binaphthyl in its supercooled melt.

Although the theory of spontaneous chiral symmetry-breaking in open systems was proposed some time ago, experimental realization of this phenomenon has not been achieved. In this article, we note that the crystal growth front of 1,1'-binaphthyl shows many of the characteristics of an open system in which chiral symmetry-breaking has occurred. We studied the temperature profiles of the crystallizing surface and obtained X-ray diffraction data of the crystals grown from the melt under controlled conditions. The data show that, under appropriate conditions, the observed bimodal probability distribution of enantiomeric excess (ee) with maxima approximately 60% is due exclusively to chiral crystals and not due to racemic crystals of 1,1'-binaphthyl that can also form at large supercooling. The mass independence of the ee shows that the growing front maintains a constant ee, which is a clear signature of open systems in steady state. Chirality 16:131-136, 2004.

Generation of molecular chiral asymmetry through stirred crystallization.

In our earlier work we established that stirred crystallization of achiral compounds that crystallize in enantiomeric forms result in spontaneous chiral symmetry breaking. The asymmetry thus spontaneously generated is confined to the solid state. In this article, we present a case in which the crystal enantiomeric excess (CEE) can be converted to molecular enantiomeric excess (EE) through a solid state reaction which relates the enantiomeric form of the crystal to the enantiomeric form of the product. Such a process not only provides a means of detecting the CEE generated in stirred crystallization but it is also a means through which chiral asymmetry generated spontaneously is "propagated" to generate chiral compounds with enantiomeric excess.

Probability distributions of enantiomeric excess in unstirred and stirred crystallization of 1,1'-binaphthyl melt.

Crystallization of 1, l'-binaphthyl from its melt can generate optical activity spontaneously. Since crystallization is a stochastic process, the enantiomeric excess (ee) generated in each crystallization varies randomly. We investigated the qualitative features of probability distribution of the ee for crystallization at two temperatures, 150 degrees C and 152 degrees C, at which conglomerate crystallization occurs. No clear transparent crystals were produced at either temperature, indicating that the solid states formed in the melt were polycrystalline. The ee randomly fluctuated from run to run, with an average of 26.9% and 2.7% when the crystallization was carried out at 152 degrees C, and 150 degrees C, respectively. The spread of the probability distribution is also substantially different. We also studied the probability distribution of ee in stirred crystallization at different stirring RPM. The results show probability distribution's broadening and evolution to a bimodality with increasing stirring RPM--a typical behavior in symmetry-breaking transitions. These results shed light on the nature of enantioselectivity in secondary nucleation and crystal growth.