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Reactive Oxygen Species Signaling Pathways: Comparison
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Please note this is a comparison between Version 2 by Camila Xu and Version 1 by Neil Blackstone.

Early in an evolutionary transition, bioenergetics and reactive oxygen species (ROS) may play a large role in managing these evolutionary conflicts. Chemiosmosis can be thought of as a poorly insulated wire—when supply exceeds demand, electrons are cast off and can form ROS. ROS signaling may thus lead to the dispersal of the excess products into the environment. These products may lead to groups and the formation of higher-level units that can subsequently be targeted by selection.

  • chemiosmosis
  • chloroplasts
  • corals
  • dinoflagellates

1. Introduction

In evolutionary biology, studies of cooperation have a lengthy and perhaps contentious history (e.g., [1,2,3][1][2][3]). While initially regarded as of less than general interest [4], as evolutionary biologists examined the history of life, cooperation was deemed to be more-and-more essential [2]. Remarkably, throughout this history, higher-level units (e.g., eukaryotic cells and multicellular organisms) emerged by the banding together of lower-level units (e.g., prokaryotic and eukaryotic cells) [5,6,7][5][6][7]. Parallels to these ancient events can be seen in a number of modern symbioses as well as simple multicellular organisms. Both symbiosis and multicellularity, whether leading to minor or major transitions, are fraught with evolutionary conflict, and these conflicts are a major obstacle for the higher-level unit to emerge.
Fundamental evolutionary conflicts can be described rather simply. As individuals form groups, some will contribute to group-level tasks (cooperators), while some will not (defectors) [8]. By shirking group-level contributions, defectors allocate more energy into their own replication and can outcompete cooperators. Mechanisms of conflict mediation have been credited with alleviating these evolutionary conflicts and preventing the competitive exclusion of cooperators [9,10][9][10].

2. ROS as Indicators of Metabolic State

Chemiosmosis refers to a process of energy conversion used by virtually all living cells and organisms. Large, metal-containing protein complexes (the electron transport chain), embedded in a membrane that is impermeable to protons, pass electrons from one to another and in the process, extrude protons. These protons then return through the membrane via ATP synthase and trigger the formation of ATP. The electron transport chain in its entirety serves as a mechanism that chemiosmotic cells and organisms can use to sense their environment. This environmental sensing in turn adjusts a variety of cellular and organismal responses. Foremost in this regard, the electron transport chain links what are ultimately environmental sources and sinks of electrons (e.g., reduced carbon and oxygen). In mitochondria, for instance, reduced carbon is oxidized and coenzymes (e.g., NAD+ and FAD) are reduced. These coenzymes are then oxidized by components of the electron transport chain which in turn become reduced. As electrons are passed between complexes, this process of oxidation and reduction continues. Finally, at least in most mitochondria, the electrons are deposited on molecular oxygen, which is reduced to water. Essentially the same process occurs in chloroplasts, although beginning with removing electrons from oxygen (which requires light energy) and ending with depositing these electrons on carbon dioxide. Bioenergetic metabolism thus links external electron sources and sinks through a series of living redox couples [22][11]. This has been a common theme since before the last common ancestor of all life, and it highlights the crucial mechanism that organisms use to detect features of the environment. For instance, if the coenzymes are oxidized (e.g., NAD+, FAD, and NADP+), the organism is running out of substrate, and this will be indicated in various ways, e.g., the ATP/ADP ratio approaches zero. Successful organisms have quickly responded to such signals for thousands of millions of years (e.g., by feeding or initiating light capture). On the other hand, if most of the coenzymes remain reduced (e.g., NADH, FADH2, NADPH), various other responses may be indicated. The number of electron transport chains may be insufficient for the available food or light and transcription and translation may ensue. Alternatively, the terminal electron acceptor (e.g., oxygen, NADP+) might be scarce. Several organismal responses might ensue, involving behavior and locomotion (e.g., movement), physiology (e.g., respiration), or development (e.g., angiogenesis). In some cells, a switch to an alternative electron acceptor may be initiated. In the case of photosynthesis, end-product inhibition may be occurring, provoking a variety of responses. In these and many other circumstances, living things employ this sort of “redox” signaling as a rapid and effective mechanism to adjust bioenergetic metabolism to environmental conditions. Throughout the history of life, the “payoff” has been a larger dividend of energy. Since this dividend can be spent on a higher rate of replication, the Darwinian imperative is clear. In eukaryotes, such redox signaling is often accomplished by intermediaries such as ROS (broadly defined here as partially reduced forms of molecular oxygen such as hydrogen peroxide and superoxide [19][12]). For example, if the environment becomes stressful and thus unfavorable for cellular replication and other energy-demanding activities, yet plenty of substrate remains available, cellular metabolic demand may diminish, and the ATP/ADP ratio may approach one. Nevertheless, oxidation of substrate may continue until the trans-membrane electrochemical gradient reaches a maximum, and the membrane-bound electron carriers become highly reduced. In such circumstances, these electrons carriers may donate electrons to molecules (e.g., molecular oxygen) whose partially reduced products can serve as messengers (e.g., ROS) [23,24,25,26][13][14][15][16]. These messengers can then trigger the appropriate adaptive response at the cellular level [27,28,29,30,31,32,33][17][18][19][20][21][22][23]. On the other hand, during starvation the ATP/ADP ratio may approach zero, and the trans-membrane electrochemical gradient may become minimal. The electron carriers may now be relatively oxidized and formation of, for example, ROS also becomes minimal. Again, appropriate responses can subsequently be triggered. Conveniently, ROS are ephemeral so their signaling can be rapidly tuned to changing environmental conditions. In this context, note that cells have a number of specialized redox proteins to modulate signals generated with ROS (e.g., thioredoxins, glutaredoxins, and peroxiredoxins [34][24]). Energy metabolism itself can be adjusted to modulate the signaling microenvironment. For example, glycolysis can follow the canonical path to pyruvate or divert substrate in a number of ways, including most notably the pentose phosphate pathway, generating NADPH to counter oxidative stress [35][25]. The latter may have dramatic effects on organismal disease and longevity [36,37][26][27]. While the signaling pathways may have a variety of subtleties and complexities, it is the ROS that activate the pathways and lead to the outcomes. Much early research on ROS focused on the toxicity of high concentrations of these molecules [38][28]. It has become increasingly clear, however, that ROS also have important functions in within- and between-cell signaling. It would nevertheless be misleading to imply that ROS are always harmless. As described by Brownlee [39][29]:
“Diabetes-specific microvascular disease is a leading cause of blindness, renal failure and nerve damage, and diabetes-accelerated atherosclerosis leads to increased risk of myocardial infarction, stroke and limb amputation. Four main molecular mechanisms have been implicated in glucose-mediated vascular damage. All seem to reflect a single hyperglycaemia-induced process of overproduction of superoxide by the mitochondrial electron-transport chain. This integrating paradigm provides a new conceptual framework for future research and drug discovery.”
Under most physiological conditions the signal encoded in ROS is read and reacted to before significant damage can occur. It is in this context that ROS signaling pathways may function as arbiters of evolutionary conflict. This hypothetical relationship is elucidated by the examples that follow.

3. Corals and Dinoflagellates: ROS Signaling in a Modern Symbiosis

Numerous marine animals form symbiotic associations, particularly clonal and colonial representatives of taxa such as sponges, ascidians, bryozoans, and cnidarians [40,41,42,43][30][31][32][33]. Remarkably, all modern reef-building cnidarians contain endosymbiotic dinoflagellates [44][34], formerly referred to as Symbiodinium and now classified as the family Symbiodiniaceae [45][35]. Many other colonial cnidarians, whether part of coral reef communities or not, also exhibit symbioses with various forms of Symbiodiniaceae. The coral-dinoflagellate symbiosis has attracted considerable attention because its breakdown seems to be integral to coral bleaching. When environmental stress (e.g., light and heat) becomes extreme, corals bleach, thus indicating that these dinoflagellates have been lost [46][36]. As elaborated below, ROS signaling likely alleviates evolutionary conflicts, but also contributes to the process of coral bleaching in which the cooperative symbiosis breaks down. While taxa included in the Symbiodiniaceae form symbioses with corals and many other metazoans, they also remain capable of free-living existence. Given the intense competition for space in marine benthic communities, symbiosis appears to be a path by which Symbiodiniaceae can become larger and thus more effective competitors. In parallel, size increase also seems to have been central to the origin of eukaryotes and multicellularity (18). For the metazoan host of Symbiodiniaceae, the symbiosis provides at least partial autotrophy, since these dinoflagellates are photosynthetic and actively export various forms of reduced carbon to the host [46][36]. Despite these mutual benefits, robust mechanisms of conflict mediation are needed to produce a durable symbiosis and to hold defectors in check. For instance, a structured population consisting of many, small groups can mediate conflict. Even if defectors are strongly selected at the individual level, with many, small groups, purely by chance (i.e., genetic drift) some groups will comprise only cooperators. At the higher level, these groups of cooperators will be strongly selected for and outcompete groups that include defectors. This sort of scenario likely contributed to numerous evolutionary transitions, including the secondary symbioses that gave rise to dinoflagellates [11][37]. While some stages of the life cycle of colonial cnidarians may comprise many small groups (e.g., when small, sexually produced colonies first take up symbionts [47][38]), overall populations of colonial cnidarians are structured entirely unfavorably in this respect. Indeed, these populations can be characterized as relatively few very large and very long-lasting groups. In other words, cnidarian colonies are large, long-lived, and relatively scarce, and a single colony contains many trillions of symbionts. Within a colony, under these conditions defecting symbionts are strongly selected for. A stable symbiosis cannot be achieved without additional mechanisms to mediate evolutionary conflicts.

4. Eukaryogenesis: The Role of ROS in a Major Transition

The most challenging of all the major evolutionary transitions appears to be the origin of eukaryotes [78][39]. Certainly, all evidence suggests a long period in which life on earth was dominated by prokaryotes. What were the obstacles that hindered this transition for 2 billion years? While we may never completely comprehend the answers to this question, there can be no doubt that evolutionary conflict was a serious hurdle. Metabolism in general and chemiosmosis in particular likely had crucial roles in mediating these conflicts. The advantages of eukaryotic cells are straightforward. Not only are they more complex, but they are also larger than their prokaryotic forebearers. As Bonner [79][40] points out, “…the reason for non-stop selection for organisms of increased size is that the top of the size scale is an ever-present open niche and has been open during the entire course of organic evolution”. Larger size provides a number of ecological advantages including the exploitation of more and different food resources, more efficient dispersal (e.g., escaping the constraints of low Reynolds numbers), producing more offspring, and escaping predators [80][41]. Prokaryotes, however, face a conundrum that greatly limits their options for size increase: their energy-converting complexes are found on the cell membrane [81][42]. If a prokaryotic cell gets larger, there is less surface to convert energy and more volume requiring energy conversion. Despite some exotic exceptions, by-and-large prokaryotes never transcended these surface-to-volume constraints. One way to circumvent these constraints is to move small energy-converting cells inside a larger complex cell, thus freeing the external membrane from duties related to energy conversion [81,82][42][43]. This arrangement allows for the complex cell to increase in size. From this perspective, endosymbiosis is integral to the evolution of eukaryotes [83][44]. A clever engineering solution for surface-to-volume constraints, however, results in a levels-of-selection nightmare. This can be better understood by recognizing the fundamental duality of life. All life takes up energy from the environment and typically converts this energy into more useful forms. At the same time, life involves information and replication. There remains a constant tension between these two attributes in all forms of life. In a structured population, a biological unit that relies on its sister units for energy conversion and specializes in replication may be favored. The success of such a unit, however, is frequency dependent [7]. As the proportion of units specializing in replication increases within a group, the availability of the products of energy conversion inexorably decreases. At some point, the lack of these products threatens the entire community. For the community to persist, mechanisms of conflict mediation must evolve. While these issues prevail throughout the entire history of life, they were particularly acute in the origin of the eukaryotic cell. Two great symbioses—that of the mitochondrion and the plastid—figure prominently in the rise of eukaryotes. Both of these symbioses involve energy-converting lower-level units, with groups of these lower-level units and host cells constituting the higher-level units. In both cases, evolutionary conflict no doubt involved the usual pattern of lower-level units specializing in replication at the expense of distributing the products of energy conversion to the higher-level community. Mitochondria may have been attendant to the very early stages in eukaryotic origins and were very likely a feature of the last eukaryotic common ancestor (LECA) [84][45]. Plastids were acquired by some eukaryotes not long after LECA [85,86][46][47]. The origin of eukaryotes continues to be one of the most debated topics in all of biology. Considerations have turned to the nature of the original host and metabolic relationships that may have led to the endosymbiosis, topics that continue to attract considerable attention and sometimes sharp disagreements [87,88,89,90,91,92][48][49][50][51][52][53]. In modern eukaryotes, evolutionary conflict is mediated by a number of mechanisms (e.g., the nearly complete loss of organellar genomes). Nevertheless, the evolution of many of these mechanisms required strong selection on the higher-level units. Such selection cannot have molded the initial steps in the symbiosis, which by definition involved only lower-level units. Notably, mitochondria, chloroplasts, and their bacterial relatives convert energy using chemiosmosis, which involves electron flow and proton extrusion as described above. The discovery of quantum electron transfer in biological systems [93][54] occurred contemporaneously with the development the chemiosmotic theory [94][55]. Later work showed that membrane-bound electron carriers could form “super-complexes.” Both quantum electron transfer and super-complex formation result in extremely rapid electron transfer in chemiosmotic processes [95,96][56][57]. When chemiosmosis is linked to the soluble reactions that store energy, this rapidity poses problems. For example, the ATP and NADPH produced by chemiosmosis in chloroplasts is stored by RuBisCO and other Calvin Cycle enzymes by reducing carbon dioxide. RuBisCO is thus the most abundant protein on Earth. The channeling of chemiosmosis into slower soluble reactions with potentially limited storage capacity has other effects. As pointed out above, if products cannot be consumed or stored and their accumulation inhibits electron flow, electron carriers become highly reduced, and these electrons may divert to molecular oxygen forming ROS. The chemiosmotic process itself, by separating protons and electrons, is the cause of ROS formation. Cooperation is not an automatic outcome of evolutionary interactions because it often involves costs. Selection may thus favor incompatible features of hosts and symbionts [97][58]. A symbiont may be selected to defect, e.g., by hoarding resources obtained from the host and symbiont community and using these resources for its own replication. While cooperative symbionts at least in part forgo reproduction and share resources with the larger community, defectors may gain a replicatory advantage by sequestering these resources. Yet, by sharing resources with the host, the cooperative symbiont community may establish a durable environment and insure its long-term persistence. Even with these long-term advantages, the higher-level unit (the host and the larger symbiont community) may be exploited by lower-level defectors. While symbiosis can be classified as mutualistic or parasitic (i.e., in bilateral terms), mechanistically these evolutionary interactions are multilateral and multilevel. Defecting symbionts can still arise and flourish even when a host-symbiont community appears to be dominated by mutualistic interactions. Mechanisms of conflict mediation are always necessary to control lower-level defectors. A structured population may mediate conflicts, e.g., if a population is subdivided into many small groups. These groups can lead to kin selection and reciprocity. Further, groups of cooperators can arise purely by chance. In this way, even if cooperation is selected against at the level of the individual, it can still arise and be favored at the level of the group [11][37]. Remarkably, ROS signaling pathways may serve as arbiters of evolutionary conflict. Chemiosmosis proceeds rapidly and conserves a large proportion of the energetic input, quickly generating products. The products of chemiosmosis may be stored, but storage mechanisms can be slow relative to chemiosmosis. Additionally, storage capacity is not unlimited. When conditions are favorable, chemiosmotic cells and organisms are often confronted with “end-product inhibition” [56[59][60][61][62],57,58,98], which can have detrimental consequences. As discussed above, an overabundance of product can inhibit electron flow. In the presence of molecular oxygen, this enhances the formation of ROS. Such partially reduced forms of oxygen can have a variety of deleterious effects. To avoid blocking electron flow, the abundant products of chemiosmotic energy conversion must be consumed, stored, or simply gotten rid of. While mechanisms that modulate chemiosmosis are available [99,100][63][64], alternatively the products of chemiosmosis can be dispersed into the environment. Because ROS are ephemeral, they are particularly well suited for this role. With the onset of end-product inhibition, ROS would increase, possibly signaling the initiation of the export of chemiosmotic products. As these products were exported, end-product inhibition would lessen, and ROS would rapidly subside. Crucially, chemiosmosis and its consequential ROS formation can thus under some circumstances favor sharing rather than hoarding the products of energy conversion. Sharing can lead to the formation of groups, whether symbiotic associations or multicellular aggregations. These can be thought of as a by-product of sharing, which in turn is a by-product of chemiosmosis. Thus formed, these groups may be the key to the evolution of cooperation, potentiating kin selection, reciprocity, or group selection. Indeed, the biophysical constraints of chemiosmosis may have provided the initial mediation of conflicts associated with origins of eukaryotic cells and thus allowed the first steps in the formation of complex life on Earth. Mechanisms that mediate evolutionary conflict typically constrain the variation at the lower level, so that defectors are less likely to evolve, or increase the variation at the higher level, so that cooperative groups are favored by selection [9,10][9][10]. ROS signaling pathways may or may not fit this paradigm. If a pathway leads to cell death, it constrains variation at the lower level. On the other hand, if a pathway leads to nutrient export and group formation, this clearly does not constrain lower-level variation. By leading to group formation, it may, however, be viewed as increasing the variation at the higher level. Depending on which pathway(s) are activated, ROS could lead to one or the other. Hence, as further discussed below, ROS are termed “arbiters” of evolutionary conflict to better represent their putative role in initiating a signaling process that resolves conflict and leads to the emergence of a higher-level unit. As endosymbioses became established and higher-level units emerged, energy-converting lower-level units remained an obstacle to cooperation. Numerous additional mechanisms of conflict mediation subsequently evolved, facilitated by the large populations of higher-level units, which each contained relatively small populations of lower-level units. Purely on the basis of chance, some higher-level units could be formed from cooperative lower-level units. These groups of cooperators could then outcompete cells that included one or many defectors. Nevertheless, under conditions that lead to end-product inhibition, defectors that arise via loss-of-function mutations could still be eliminated from cooperative groups. In this way, unicellular eukaryotes developed robust and stable symbioses. The biophysics of chemiosmosis, particularly the formation of ROS as a by-product, were likely central to the initial steps of eukaryogenesis, when only lower-level selection was operating. Both quantum electron transfer and super-complex formation contribute to high rates of chemiosmotic processes. Large quantities of products may thus be produced. While several mechanisms can modulate chemiosmosis, alternatively excess product can be released, thus providing a way to protect against an accumulation of end-products and the consequent formation of dangerous by-products such as ROS. Sharing may thus occur with little cost and considerable benefit—"the free lunch you are forced to make” [16][65]—thus facilitating groups. Such groups can lead to cooperative symbioses. Even after such groups have formed, however, cooperators are always vulnerable to exploitation by defectors, so additional mechanisms of conflict mediation are usually necessary. While there are examples of prokaryotic aggregations (e.g., biofilms), these pale in comparison to eukaryotic multicellularity (e.g., Conway Morris [101][66]: “The history of life shouts ‘Look! Once there was bacteria, now there is New York’”). Eukaryotes seems particularly able to form complex, multicellular organisms. Possibly, the mechanisms of cooperation established by the eukaryotic cell may have been repeatedly co-opted during the emergence of eukaryotic multicellularity [102][67]. In multicellular organisms, the result may be fundamental relationships between nutrient supply, metabolism, and cooperation that are only now beginning to come into focus [16,17,18][65][68][69].

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