Eumelanin in the Living World: Comparison
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Please note this is a comparison between Version 2 by Sirius Huang and Version 1 by Maria Letizia Terranova.

A lot of still unexplained aspects characterize eumelanin, a macromolecule able to play in living organisms several , sometimes conflicting, roles. This contribution  aims  to  emphasize the unique characteristics  and the consequent  unusual behaviors of a molecule  that in an evolutionary context  survived natural selection and still holds the main  chemical/physical  features detected  in fossils dating to the late Carboniferous. 

  • eumelanin
  • resilience to  diagenesis
  • stress responses
  • radiotropism
  • radioprotection
  • anti/prooxidant roles
  • semiconducting properties
  • paramagnetic behavior
  • redox properties

EUMELANIN in the LIVING WORLD

 

1. Introduction

No other natural polymer is characterized by so many intriguing properties and is able to fulfill such a wide variety of different functions as eumelanin (called henceforth EU), which is the dark-brown/black component of the melanin family. A lot of unique characteristics make this biopolymer very different from almost every other macromolecule, including the orange-red pheomelanin, the other form of natural melanin.

2. The Ubiquity in the Living World

EU is the unique biopolymer widespread in all the biological world, from vegetables to bacteria, from insects to the more complex animal kingdom, from invertebrates to vertebrates. It is found in fungi, cephalopods, birds, and mammals, just to name a few. In the more complex organisms, EU is present in various organs and plays a variety of roles. As an example, in mammals, EU and its derivatives are found in “substantia nigra”, “locus coeruleus” and “medulla oblongata”, areas of the brain where a series of fundamental neurological functions occur [35][1]. Here, EU plays a role in neurotransmission and regulates the accumulation of toxic metal ions [36][2]. The EU pigment is found also located in the retina of the eye and in the cochlea of the ear, where it governs the transmission of functional signals.

The chemico/physical analytical approaches developed in the last two decades have enabled unambiguously identifying the presence of EU also in ancient species and to compare the composition of pigments preserved in the fossil record with those extracted from the latest living organisms.

3. The Keeping over Times of Chemical/Physical Features

The impressive preservation of EU over geological time scales is a further interesting feature of this pigment. The highly efficient microbial decomposition does not allow in general the preservation of soft tissue in the fossil record [37,38][3][4]. The organic constituents of soft tissues are indeed subjected to diagenetic alterations, i.e., biological and physicochemical degradation processes that cause their transformation into hydrocarbon chains [39][5], and they are rarely preserved in fossils more than 65 Ma old [40][6]. However EU has been detected in the ink sacs of coleoid cephalopods dating back to Early Jurassic [41][7], in fossils about 200 Ma old [42][8] and also in samples dating to the late Carboniferous, ~307 Ma ago [43][9]. Appropriate technologies have recently enabled to analyze the physical/chemical characteristics of the fossilized pigments and to confirm the exceptional resilience to diagenesis and the long-term preservation of EU, which are characteristics that distinguish this complex biopolymer from every other biomolecule.

The animal EU is generated by melanocytes, cells able to synthesize the enzyme tyrosinase, and it is contained almost exclusively in lysosome-derived vesicles with a diameter of about 500 nm, which are called melanosomes [44][10]. Melanosomes are typically found in integumentary structures (feather, scales, skin, hair) of various amniote lineages, from sauropsids (reptiles, birds, non-avian dinosaurs) to synapsids (including mammals) [45,46,47][11][12][13] and distributed in different body tissues and organs of vertebrates and invertebrates [43,48][9][14].

The size and shape of melanosomes detected in the fossilized invertebrates are similar to those present in the extant ones, as confirmed by studies performed on coleoid Sepia Officinalis [49][15]. As regards the vertebrates, fossilized melanosomes have been found also in the retina of the eye, in the inner ear, in some regions of the brain and in other organs [35,50][1][16]. A correlation between the external (integumentary) and internal (organs) amount of EU present in living species has been outlined in [51][17].

The large amount of data obtained from a variety of fossil vertebrates from Carboniferous to Pliocene enables nowadays to hypothesize the possible functions exerted by EU in ancient organisms [46,52][12][18].

A deep review reporting and discussing what is presently known about the localization of melanosomes and possible functions in major vertebrate classes has been recently published by Mac Namara et al. [53][19].  It has also been speculated that the history of EU could be backdated up to the prebiotic era [54][20]. Structural features and physicochemical properties of the melanin found in some living organisms, such as bacteria and fungi, show indeed several analogies with those of the insoluble organic matter found in carbonaceous chondrites, dating 2–4 Ma from the Solar System formation [54][20].

4. The Ability to Withstand Extreme Conditions

The ability of living organisms to synthesize eumelanin imparts a selective advantage in surviving and growing under extreme environments. A striking example is given by the melanized black fungi, which withstand extreme chemical/physical conditions and resist multiple stresses [55][21]. The outstanding ability of EU to resist the alterations has been tentatively ascribed to the highly cross-linked original state of the biopolymer [39,40][5][6]. However, other properties specific to this intriguing macromolecule, such as the complex radical system and the peculiar redox responses, also account for the superior resistance to stresses.

There are several strategies conceived by EU to overcome stresses and to increase the viability of species either living in harsh environments or anyway needing to counteract adverse effects. Stresses include, beyond oxidant agents, extreme temperatures, freezing/defrosting cycles, dryness, changes in osmotic pressure, microbicidal drugs, and the immune response of host organisms. To increase their tolerance to any negative impact, the melanized species react by putting in place the same front-line strategy, namely the boosting of EU production [56][22].

Examples are given by the human pathogenic Cryptococcus neoformans, Wangiella Dermatitidis, Sporothrix schenckii, Aspergillus fumigatus, Histoplasma capsulatum  and by some phyto-pathogenic fungi, against which the immune systems of the organism under attack implement a defense strategy based on the rapid production of reactive oxygen species (ROS). To counteract the oxidative burst and to maintain/increment the virulence in the host organism, the pathogens increase the EU production. In such a way, at the site of attack, the EU’s efficient system of free radical quenching is able to activate a strong reaction [55,57][21][23]. The protective effects of EU against oxidative stress extend to all kinds of reactive species, from singlet oxygen [58][24] to radicals associated to the excited states of dye molecules [59][25] and also to those generated by non-photic stimulations [60][26].

In addition, the great ability of EU to bind redox-active metal ions and oxides is implemented by a variety of organisms, from bacteria to mammals, that utilize the metal uptake process to contrast cytotoxic effects [61][27].

Due to the effective interaction with metal ions, this biopolymer can exert also a protective function against lipid peroxidation [60][26]. This further role of EU was discovered when in vitro studies of pigmented and unpigmented liver tissues evidenced the ability of EU to inhibit lipid peroxidation induced by Fe2+  ions [62][28] and also the peroxidation of cardiolipin liposomes induced by Fe2+-ascorbic acid [63][29]. A very complete review of the effects produced in living organisms by the EU–metals interactions can be found in [21][30].

The stress-induced increase in EU production results also in a decrease in cell permeability, which was an additional defense mechanism for melanized species living in challenging chemical environments. The greater amount of melanin granules increases the cross-linking of the cell walls, significantly reducing the pore sizes and therefore the cell permeability [64,65][31][32]. This feature is particularly exploited by melanized species that survive and flourish also under hypersaline conditions [66][33]. In this case, the increased amounts of EU accumulated in the cells implement an osmo-adaptative strategy that reduces the loss of protective substances from the cell walls [55][21].

However, the most dangerous among the various stress factors to deal with when survival is at stake is the exposition to high doses of ionizing radiations. In this context, EU shows a further unique feature, i.e., the capability not only to withstand highly ionizing radiations but also to take advantage of them. This functionality distinguishes EU from every other biomolecule, including the also long-surviving chitin and collagen.

The unexpected growth of black fungal colonies exposed to high-level of ionizing radiations observed in Nevada nuclear test sites [67][34], in areas contaminated by nuclear fallout [68][35] and in nuclear reactor waters [69][36], has been fully understood in the 1990s, when Russian researchers deeply investigated the behavior of Cladosporium sphaerospermum  Cladosporium sphaerospermum fungi growing in the highly radioactive areas surrounding the damaged Chernobyl Atomic Energy Station [70,71][37][38].

The analysis of the pigmented fungal species thriving in either natural highly radioactive environments or in environments contaminated by anthropogenically originating radionuclides disclosed that, in all cases, such species had a high content of EU. A proof that EU was able not only to assure the viability but also to increase the metabolic activity of living species containing DHI and DHICA oligomers was obtained later by comparing EPR spectra of melanized and non-melanized species exposed to controlled doses of β and γ radiations [23,72][39][40].

The significative features detected in the EPR spectra of irradiated cells prompted researchers to investigate more deeply the radiation-induced changes of the EU electronic structure and to study the effects of electron transfer and paramagnetic properties modifications on the viability of melanized species. The EPR analysis performed on the C. neoformans  C. neoformans cells outlined the occurrence of a stable free radical population with two distinct paramagnetic centers [13][41], evidencing an unusual complex radical system that has been more recently verified in both natural and synthetic EU [14,73][42][43].

Experiments performed on various synthetic EU had demonstrated that even high doses (300 Gy) of γ-rays produced by a 137-Cs source did not change the quantity of the stable free radicals, indicating that the ionizing radiations do not generate in the molecule new free radical species [74][44]. Moreover, it has been proven that radiation exposure affects the redox potential of EU and causes an electron transfer that maintains the polymer in a constant oxidation state. This prolonged oxidation results in a current production and in an extended redox cycling capacity [75][45]. Further investigations have pointed out that EU extracted from irradiated cells acts more efficiently as electron-transfer agent, increasing the transfer velocity up to four times compared to the unexposed ones [76,77][46][47].

Whereas all these findings helped to interpret the behavior of irradiated EU, a more complete understanding of the protective functions exerted by EU has been reached by considering the occurrence of a further phenomenon, the Electron Compton Scattering (ECS), which is a process discovered by A.H. Compton in 1923 [78][48]. Revskaja et al. [79][49] suggested that the ECS process, i.e., the inelastic scattering of photons by charged particles, could act in conjunction with the other redox-based mechanisms to protect living species from radiation-induced damages.

The high degree of radical stability evidenced in EU under highly energetic radiations has led to the assumption that EU prevents such dangerous radiations from generating and spreading further radical species [80][50]. The most probable chemical/physical scheme is that the scattered Compton electrons dissipate energy interacting with the π-electrons rich sub-units of the EU aromatic structure, making more efficient their trapping by the stable free radicals population present in the EU backbone [81][51]. As a whole, the attenuation by Compton scattering of the energy released by high-energy radiations would impede the occurrence of secondary ionizations and the starting of the radical chains responsible of multiple DNA damages [82][52].

The extreme ability of melanin to resist radiation-induced stresses has been widely tested by exposing melanized species to different types of radiations. The highest number of experiments has been performed on the cells of the cryptoendolithic black fungus Cryomyces antarcticus Cryomyces antarcticus, which has been irradiated by high doses of x- and γ-rays [83][53], of beta particles [81][51], of alpha and deuteron particles [84][54], of He-ions [85][55] and also of accelerated Fe-ions [86][56]. These organisms, as well as other extremophilic terrestrial species such as the melanized fungus Friedmanniomyces endolithicus [87] Friedmanniomyces endolithicus [57], demonstrated not only a high tolerance to acute doses of radiations but also an increase in metabolic activity.

In addition to its singular radioprotective function, in fact, EU has been found able to convert radioactivity in energy available for metabolic processes, which is an ability termed radiotropism [88][58]. This unexpected feature has been demonstrated through a series of interesting effects, as the faster incorporation of acetate by melanized fungi under irradiation [23,89][39][59] and the upregulation, after irradiation, of ribosomal biogenesis genes in melanized yeast [90][60]. The large number of experiments performed on dark fungal species in the last few years have confirmed the radiation-induced phenomenon, ascribing the increased proliferation of irradiated species to the unusual mechanism of energy conversion put into play by EU [77,81,91,92,93][47][51][61][62][63].

What is even more interesting is that the radioprotective effect of EU, either natural or artificial, can be transferred to organisms not able to produce this biopolymer [80][50]. Higher survival rates after γ-irradiation have been indeed measured for non-melanized fungal cells grown in EU-containing cultures media and for mice models subjected to intravenous injection or the ingestion of EU [94,95,96][64][65][66].

It is noteworthy that the radioprotection conferred by EU may explain the abundance of highly melanized fungal spores found in early Cretaceous period deposits, when many other vegetal and animal classes did not survive the high radiation levels [97,98][67][68].

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