Bioelectric Fields at the Beginnings of Life
The consensus on the origins of life is that it involved organization of prebiotic chemicals according to the underlying principles of thermodynamics to dissipate energy derived from photochemical and/or geochemical sources. Leading theories tend to be chemistry-centric, revolving around either metabolism or information-containing polymers first. However, experimental data also suggest that bioelectricity and quantum effects play an important role in biology, which might suggest that a further factor is required to explain how life began. Intriguingly, in the early part of 20th century, the concept of the “morphogenetic field” was proposed by Gurwitsch to explain how the shape of an organism was determined, while a role for quantum mechanics in biology was suggested by Bohr and Schrödinger, among others. This raises the question as to the potential of these phenomena, especially bioelectric fields, to have been involved in the origin of life. It points to the possibility that as bioelectricity is universally prevalent in biological systems today, it represents a more complex echo of an electromagnetic skeleton which helped shape life into being. It could be argued that as a flow of ions creates an electric field, this could have been pivotal in the formation of an energy dissipating structure, for instance, in deep sea thermal vents. Moreover, a field theory might also hint at the potential involvement of nontrivial quantum effects in life. Not only might this perspective help indicate the origins of morphogenetic fields, but also perhaps suggest where life may have started, and whether metabolism or information came first. It might also help to provide an insight into aging, cancer, consciousness, and, perhaps, how we might identify life beyond our planet.
In short, when thinking about life, not only do we have to consider the accepted chemistry, but also the fields that must also shape it. In effect, to fully understand life, as well as the yin of accepted particle-based chemistry, there is a yang of field-based interaction and an ethereal skeleton.
Keywords: bioelectricity, origins of life, thermal vents, mitochondria, quantum mechanics, thermodynamics
In this article, we suggest that a missing factor in origins of life theories is that a flow of ions, for instance in a deep-sea thermal vent, generated an electric field, which led to a far from equilibrium dissipative self-organizing structure and a prototypical morphogenetic field putting bioelectricity center stage in the origin and evolution of life. This might suggest that the smallest quanta of life, at least on this planet, is a self-replicating and adaptive structure capable of maintaining a self-reinforcing biofield that enables the dissipation of an energy gradient, which, critically, holds information about its overall shape. From this perspective, the uncoupling of ion gradients and futile cycling can perhaps be viewed as mechanisms not only to enable dissipation, but also to maintain these fields, and so fulfil the arrow of entropy.
In relationship to genetics, it would suggest that the blueprint to build field generating structures was a latter evolutionary strategy born out of a field-driven condensation of information holding molecules that enabled true life to replicate and move beyond its birthplace. This was probably driven by changes in the local environment, in effect stress that forced natural selection.
In the “A Quantum Thermodynamic Perspective of Life” section, we review the concept that life can be explained from a quantum thermodynamic perspective, and then in the “Morphogenetic Fields and Life: An Old Idea” section, review how this leads onto why electric fields could well be pivotal. In the “Life's Origins and Charged Particle Flow” section, we then use these ideas to provide a perspective on how fields could have been pivotal in life's origins due to the movement of ions, which, potentially, favor metabolism first and thus alkaline thermal vents, and in the “From Thermal Vents to Ion Channels; In An Early Biological Dissipative Fröhlich Condensate?” section, we review how both quantum mechanics and thermodynamics could lead to more complex protein structures, which could be viewed as forms of a “Fröhlich condensate” as self-organizing resonant dissipating structures.
In the “From Prokaryotes to Eukaryotes; Cooperation, Ion Channels, and Cytoskeletons” section, we then build on these ideas by reviewing evolution from prokaryotes to eukaryotes, in particular, how the inter-relationship between fields and protein structures was key in the development of cooperativity and complexity. Finally, in the “The Ethereal Skeleton at the Beginning of Life: Conclusions and Implications” section, we discuss how these concepts could be integrated into a morphogenetic theory of life, and what the implications might be for aging, life definition, astrobiology, uncoupling, death, viruses, and the origins of cancer.
“What is life?” is a question that has been posed by many, including one of the founding members of quantum mechanics, Schrödinger.1 In fact, discussions on the role of “significant” quantum effects in biology were also undertaken by Niels Bohr and Pascual Jordan in the 1930s.2,3 This is perhaps hardly surprising, as it is generally agreed that the best description of our universe, and thus the life within it, is based on quantum mechanics and quantum field theory (QFT).4 However, before quantum mechanics, the discipline of thermodynamics was developed ostensibly to help better understand steam engines, but soon led onto concepts like entropy.5
Ever since quantum mechanics was developed after Einstein suggested, in answer to the black body radiation problem that electromagnetic (EM) radiation was quantized, the two ideas existed side by side and were often treated as separate subjects; more recently, however, with the development of new technologies, the field of quantum thermodynamics is now striving to bring the two together.6 In fact, the concept of dissipative adaption of thermodynamic systems is now being extended into the quantum realm, hinting at a quantum thermodynamics of driven self-organization.7
Overall, it is now becoming broadly accepted that thermodynamics must have played a role in the origins of life,8,9 as has a role for quantum mechanics and a universal mechanism of charge transport.10 In that light, perhaps one of the most famous quotes in biology, attributed to Albert Szent-Györgyi that “life is nothing but an electron looking for a place to rest,” which captures the importance of charge flow perfectly and has been used in origins of life theories,11 was certainly prescient as the movement of charge creates a field and is fundamental to quantum mechanics.
Thus, as life can be defined as a structure that dissipates energy by channeling ions down gradients, the fields this generates could also be part of a homeostatic feedback system as they, in turn, influence the movement of the charge. In fact, the idea that electric fields are important in biology is far from new.
At around the same time as quantum mechanics was being developed in the early 20th century, others, such as Alexander Gurwitsch, were trying to answer fundamental biological questions about how the shape and growth of organisms were controlled. This gave rise to the idea of morphogenetic fields and the role of bioelectromagnetic and photobiological factors in the structural organization of biosystems. This has since grown to embrace many different scientific disciplines, including quantum mechanics, nonequilibrium thermodynamics, order out of chaos theories, and self-organizational dissipative theories as proposed by Ilya Prigogine. It also gave rise to the ideas of Herbert Fröhlich about the role of biological coherence and condensates, as well as the potential importance of photonic resonance. In short, the “morphology” of life is perhaps shaped by fields, rather than genetics (this subject is reviewed in more depth in “Fields of the Cell,” edited by Fels et al.12).
As the “A Quantum Thermodynamic Perspective of Life and Morphogenetic Fields and Life: An Old Idea” sections indicate, as biology is all about charge flow, we cannot ignore the role of electric fields due to basic quantum thermodynamic principles. If so, when did charge first start to flow? Did life start, then charge flowed, or did charge flow, which kick started life? This is perhaps one of the most fundamental questions about the origins of life and whether or not electric fields may have been pivotal.
With regard to the more “standard” origins of life theories, there are many, ranging from metabolism, to proteins, to lipids, to nucleic acid first informational ideas, with initial power sources including sunlight and geothermal. Most start with simple chemicals13; in effect, life arose from geology. The debate had tended to revolve around whether the chemoautotrophic theory on the origins of life is stronger than the heterotrophic “organic soup” idea due to the nature of the free energy sources that drove the earliest anabolic reactions.14 Hence theories on the origins of life tend to broadly break down into phototrophic (driven by solar potential and the dissipation of energy as heat in oceans e.g., Michaelian15 or photosynthetically active zinc sulfide precipitated on thermal vents, e.g., Mulkidjanian16 and Mulkidjanian and Galperin17), and geotrophic, with life as a planetary process (driven by geochemical gradients18).
Another way of viewing this is that discussions have also tended to revolve around either metabolism or RNA (information) first; however, the “descent of the electron” seems to favor metabolism first. This is perhaps reinforced by the fact that all the starting ingredients can be made on earth, or in outer space—including many aromatic compounds.11 Although the metabolism first might favor thermal vents, others also suggest that a composite theory, such hydrothermal impact crater-lakes, due to the potential concentration of prebiotic chemicals, may have been a more likely site.19
However, one of the strongest theories is based on the observation that modern life uses chemiosmotic coupling and a proton gradient, hinting at the importance of alkaline thermal vents. This is very much a metabolism-first based on geological chemistry/genes later approach. Interestingly, some of the oldest known proteins, such as ancestral ATPases and energy converting hydrogenase (ECH) fit well with this, in particular, as these vents can also result in the formation of lipid membranes involving a process called “thermophoresis.”20,21 Furthermore, evidence of reflexively autocatalytic networks has also been identified in microbial metabolism, which is also consistent with an autotrophic origin of life in thermal vents, which seems to continue to suggest that autocatalytic chemical networks preceded proteins and RNA.22
In that light, it is perhaps of relevance that a recent article has also identified the ATPase as being a key determinate of tissue regeneration in relationship to a morphogenetic field generation that is conserved across kingdoms.23 Also, as suggested in alkaline thermal vent theories of the origins of life,20 the F-type ATP synthase seems to have arisen very early in evolution and is conserved across all domains of life.24
The alkaline thermal vent concept is based on the acid-base energy gradient present in the immediate post-Hadean—key in this process were catalysts based on iron-sulfur centers and the evolution of molecules such as the flavins that enabled electron bifurcation to occur.25 Critically, data now suggest that the modern successors to these, such as ferredoxin and flavin adenine dinucleotide, as well as many other proteins are reliant on electron tunneling to function26,27; tunneling in mitochondria may thus be key in the way they work.28,29 It also appears that proton tunneling is also a central component of enzyme function.30 Hence, it is possible that quantum effects were important in the origins of life.31,32
The bottom line is that as a potential starting point, alkaline thermal vents are as good a candidate as any, as extant biochemistry, ranging from energy systems involving acetyl CoA, to Kreb's cycle intermediates, Fe(Ni)S proteins to the central role of a proton gradient, could have evolved from these. Certainly, the flow of ions would have been conducive to the generation of an electric field, and because of the basic quantum nature of charged entities such as protons and electrons and their interaction with electric fields, the emerging consensus that biology is reliant on significant quantum effect would certainly support this. The thinking is now that rather than the “warm and wet” milieu of biology preventing significant quantum effects, it actually enhances it—the environment-assisted quantum transport (ENAQT) concept via a kind of resonance.33
If the alkaline thermal vent idea is correct, then charge flow may well have come first, which meant that the flow of ions could have generated significant fields resulting in an ion/field-based self-organizing dissipative system. This in turn could have acted as a “nucleus” that “condensed” the available molecules that in turn, could have further stabilized it into a structure where the energy was transferred by recognizable chemistry. So, what would have these first structures been like?
Today, it is thought that conditions in alkaline thermal vents could have led to the evolution of energy capturing ion channels, like ECH and ATPase,20,34 which could have been embedded in membranes that could have also formed under these conditions.21 In effect, some of the earliest “biotic” structures could have been something like an ion channel that “condensed” around some inorganic structure that was flowing ions and was reinforced by electric fields.
Further support for this perhaps comes from the thought that ion channels, in general, are evolutionarily very old as they are highly conserved across all kingdoms—certainly the proton pumping ATPase/synthases can be traced back all the way to the last common ancestor of all extant life, and the more modern complex versions probably arose from gene duplication events.35 Voltage-gated ion channels are also universal.36 In effect, proteins that can both extract energy from a gradient, as well as sense and control the flow of ions, had probably been a very important step in life's evolution.
It could therefore be said that thermodynamics could provide the “drive” for a dissipative structure to form by organizing existing molecules, for instance, in a membrane to form energy extracting and voltage sensing channels. Although potentially on a different scale, the ability of energy to induce a phase transition into an organized dissipative structure such as a Bénard–Rayleigh convection cell,12 which looks almost identical to an ion channel, is perhaps striking (Fig. 1). What is also relevant is that membranes can spontaneously form ion channels without the need for any proteins in the presence of an energy gradient; in effect, synthetic lipid bilayers can display many of the effects of say, transient receptor potential channels—especially near to their chain melting temperatures.37
But what other physical principles might be at play? As previously discussed, quantum mechanics has of course been long thought to be important in understanding biology.1,38,39 In fact, there is an old but highly relevant theory, developed by Herbert Fröhlich, which discusses the role of condensation in biology from the quantum mechanical perspective. In effect, this theory stipulates that energy can be stored in excited vibrational modes in cells by metabolically driven polar oscillating units involving an interaction between the very large EM field generated by a mitochondrion and the cytoskeleton, resulting in a “condensed” energy state in a mode with the lowest frequency.
Critically, the strong electric fields generated by mitochondria could also potentially organize water.40 This becomes even more relevant, in that it is entirely possible, as explained by quantum electrodynamic (QED) theory, that water itself can become coherent under certain conditions, for instance, near hydrophilic surfaces under the influence of electric fields and especially when it contains impurities. This is known as exclusion zone (EZ) or interfacial water (reviewed in chapter 5 of Fels et al.12). It has even been said that the coherent quantum frequencies of water itself could be pivotal in life.41
It is thus perhaps relevant that recent data suggest the presence of an ordered water channel in ATP synthase, which via a Grotthus mechanism, could channel protons.42,43 Furthermore, the presence of ordered water in the proton channel of a V-ATPase has also been inferred.44 Thus, the possible presence of ordered water that could enhance proton transport in such ancient and important proteins could hint at some kind of resonant condensation process involving electric fields that could be an echo of the very earliest structures as life began.
If life is dependent on a charge flow-field interaction, how might this express itself as biology evolved ever greater complexity? A key facet of this maybe that increasing complexity enabled more information to be stored, enhancing the ability to adapt to changing environments. Clearly the evolution of genes was one answer to this, but information can also be stored in networks, enabling rapid responses, for instance, in the interactive flow between ions and the fields they generate.
Data indicate that life was prokaryotic for billions of years until the union of bacteria and Archaeans led to the modern eukaryote.45 The evolution of eukaryotic multicellularity, with a means of coupling bioelectric networks, say, via gap junctions, does indicate that this cooperation was certainly a key mechanism for enhancing robustness and storing information.46 However, perhaps less appreciated is that cellular cooperation evolved long before this, and seems to have been the normal state of affairs for billions of years in the prokaryotic world: for instance, large colonies of prokaryotes seem to recapitulate phylogeny as they grow.47 Critically, ion channels could well be key in this cooperation.48 This raises the rather intriguing possibility that not only were fields essential at the beginning of life, but also that this led to cooperation. In essence, life did not evolve as a single cell, but as a cooperating group.
As discussed, ion channels appear to be pivotal in bioelectricity and are very old. However, another emerging evolutionary story is also coming to the fore, and that is prokaryotes also have cytoskeletons made up of precursors to those found in modern cells, such as tubulin and actin—which self-assemble to form polymers.49 Critically, it seems that some of these cytoskeletal elements also have enzyme function, suggesting evolution from dual-role proteins—in effect the ability of enzymes to form these polymers.50 Today, theoretical research based on the ideas of Fröhlich seems to indicate that these microtubules, certainly in eukaryotes, can exhibit super-radiance and coherent energy transfer, in effect, excitonic resonant states that are modulated by reactive oxygen species (ROS), calcium, and light, and many other chemical parameters; alterations in this system could underlie many pathological states.51 Furthermore, static magnetic fields can also affect their polymerization,52 hinting at another factor that may have been important.
In terms of more conventional biochemistry, it is well described that tubulin interacts with the voltage-dependent anion channel, a pivotal mitochondrial protein, and modulates its membrane potential—and may well play a key role in cancer.53 The key thing here is that mitochondria and the cytoskeleton are intimately and dynamically linked in function and can be spread throughout the cell—right up to the plasma membrane; certainly in neurons, they are pivotal in synapse function, for instance, for energy and calcium homeostasis.54 It now seems that not only can gap junctions be pivotal in transfer of mitochondria to other cells,55 but also via cell to cell tunneling nanotubes—which appear to be extensions of the cytoskeleton and could well be part of an electrical signaling system.56