Redox Stress Burden of Trace Metals on Environmentally Dependent Ecosystem

Abstract

Contamination of the environment by trace metals (TMs) has become a global health challenge. Some of these metals are found in some food substances in minute quantities as a normal part of nutrition. Excessive exposure of living organisms to these metals poses’ a great risk to the health of the living organisms. Once in the environment, these metals are not biodegradable and last for a long time. Their contamination of the environment leads to contamination of the ecosystem, which intricately depends on the environment. Normal physiological processes of the living organisms in these ecosystems are distorted following the dysregulation of their redox system. An imbalance in the ecosystem’s redox state led to damage to living organisms. There is an increase in mortality and morbidity, diversification is compromised, the genetic makeup of organisms is altered and over time the whole ecosystem becomes compromised. Several bioremediation techniques have been of valuable assistance in reverting this ugly trend. How well these remediation works could revert the damage and restore the ecosystems will be a measure of their survival, including all the dependent organisms and man.

1. Introduction

Trace metals (TMs), and their contamination of the environment with associated health risks is a current global environmental burden that requires urgent attention. This is a sequel to rapid urbanization, industrialization, and globalization [1]. The word TM is difficult to define and the list of metals included in this term is somehow controversial. The deleterious effects associated with TMs had been known to man since the twelfth century AD when Selenium (Se) toxicoses were recorded in livestock [2]. Before then, environmental toxicants are known, but not properly defined. For instance, the toxicities of realgar (As4S4) and orpiment (As2S3) are well known in ancient times (64–50 BC), prompting the miners to use slaves for the exploration of these metals since they know that it is associated with early death [3]. Ever since then, several environmental TM contaminations may have taken place, but not until the eighteenth century when the toxic effects of arsenic (As), lead (Pb), copper (Cu), zinc (Zn), iron (Fe) and manganese (Mn) in drinking water were established [4]. The term TM in ordinary usage refers to metals that living things (both plants and animals) require in minute (trace) amounts to maintain normal homeostasis. Chemically, TM refers to metals that are less than 100 micrograms per gram (<100 μg/g). They include approximately 47 metals, but not all are common. The most common ones that are associated with either nutrition in living things or are well known for toxicity are iron (Fe), copper (Cu), zinc (Zn), rubidium (Rb), selenium (Se), strontium (Sr), molybdenum (Mo), manganese (Mn), lead (Pb), arsenic (As), chromium (Cr), cobalt (Co), vanadium (V), and cadmium (Cd) [5]. Some sources also include nickel (Ni) and beryllium (Be). Generally, metals can be essential or non-essential. The non-essential ones like Pb, Cd, As, etc. exhibit toxicity without playing any physiological roles while the essential ones play some roles in the normal functioning of living things [6, 7]. TMs are non-biodegradable and as such last forever in the environment, exerting deleterious effects. Elements such as As, Cd, Cr, Hg, and Pb are believed to have no known physiological role either in mammals or plants. The beneficial ones only serve as nutrients in minute quantities. Excess doses beyond the requirements of living things lead to toxicity [8].

The environment in which the TMs contaminates could be divided into three parts: 1. The earth is known as the geosphere. 2. The water body is known as the hydrosphere. 3. The gaseous environment is known as the atmosphere. There is a great interaction going on between the geosphere (lithosphere), hydrosphere, and atmosphere leading to the exchange of materials and energy, TMs inclusive (Figure 1). TMs can occur in any form of matter, i.e., solid, liquid, or gas either as single metals or combined. Originally, every TM is found in the earth’s crust as metal deposits or in minute quantities in plants and animals. But, following anthropological activities, these TM find their way to the environment where they exist as contaminants. They get to man via food, inhalation, water, or direct contact with the body. The chemistry of TMs made it such that they are non-biodegradable, and as such once in the environment, they exist for ages. Some micro-organisms though may partially detoxify these TMs by taking them up in some of the protein moiety that has an affinity for TMs and storing them there for long periods [9].

Figure 1.

Schematic description of the trace metal interaction between the geosphere, atmosphere, hydrosphere, and biosphere.

1.1 Trace metals: a source of environmental contamination

Contamination of the geosphere, hydrosphere, and atmosphere ultimately leads to contamination of the biosphere, the dwelling place of living things. The biosphere is the primary environment where humans, animals, plants, and microorganisms dwell, live, work and interact within themselves and with the environment [10]. The last millennium saw an upsurge in the anthropological activities of the earth’s crust as a way of meeting up with the increasing demand for products involving metals as raw materials or used in their manufacturing process. Other sources like poorly maintained vehicles, volcanic eruptions, and agricultural chemicals like pesticides, insecticides, and fertilizers also contribute to the TMs source [1]. While increasing care in metal exploitation following legislation has reduced the level of contamination, careless disposition and unintended contamination had increased metal flux in the environment [11]. The resultant effect is an environment defiled with TMs, leading to disruptions in natural habits and its dependent ecosystem. The forces of inter and intra-compartmental exchange of TMs make exchange between one compartment to another easy. The chemistry of these TM is such that they easily form covalent bonds with organic materials leading to the formation of secondary compounds with lipophilic properties. They also form compounds with non-organic materials resulting in increased toxicity to living things. Because of this ability to form different compounds of different chemical classes, toxicity arising from the TM in the biosphere differs from simple surface allergies to complex distortions in enzymes, and proteins and damage to DNA [12, 13]. Compounds like tributyltin oxide and methylated As are easily found in the environment and are very toxic to the ecosystem. TMs like Hg or Pb has a very high affinity for sulfhydryl groups of thiol proteins [9].

Following contamination of the biosphere, movement from one area to another depends on the interplay of the water body and air movement, the temperature of the environment, polarity, partition coefficient, pressure, and stability of the element [14]. Contamination of the soil with TMs can lead to entrance into the ecosystem by way of plant absorption and magnification and subsequent transfer to higher troughs of the ecosystem which will eventually get to the man. TMs can also alter the chemistry of other environmental pollutants that hitherto were more degradable, making them less degradable and increasing both the lifespan in the environment and the duration of toxicity [14, 15]. Contamination of the water body from industrialization and urbanization ends up in bigger water bodies like the ocean where aquatic dependent species accumulate these TMs and pass them along the ecosystem. The toxicity to aquatic organisms depends on the chemistry of the TM, the physiological role of the TM, the nature of the organism, the duration of exposure, and the health state of the organism [16]. TMs even at very low dose in the aquatic system is deleterious to aquatic animals since factors like salinity, pH, and other concomitant pollutants in the water bodies like microplastics affect their toxicity [17]. Once an edible aquatic animal is contaminated, it passes it along the food chain until it eventually gets to man, the ultimate sufferer of the poison because of bioconcentration. Some TMs like Cd, nickel, arsenic, beryllium, and chromium are known for their mutagenicity, carcinogenicity, and teratogenicity [18]. Since there is usually a high level of TMs in the sewage leading to contamination of water bodies, proper treatment of the sewage to remove TMs leads to healthier water bodies and their associated ecosystem. This can be achieved with stringent regulations using improved technology [19]. TMs can settle on the surface of water or form a solution with water or settle to the bottom of the water along with particulate matter (PM). Urbanization and industrialization have also affected greatly TMs contamination of the air especially latching to particles where the wind can convey it long distances away from the primary source of contamination [6]. TMs can get adsorbed on particles to form a metal-particulate complex that can be transported by wind to the non-contaminated area [20]. The atmosphere is made up of different layers and each can be affected differently. The troposphere and the stratosphere are the worst hit since they are the ones above the immediate earth with a lot of swirl wind exerting mixing pressure within it [21]. TMs distribution in the air of a particular area depends on the predominant activity in that area. For instance, a high vehicular traffic area is usually dominated by Pb, while the ceramic industrial area is contaminated with As [22, 23]. Furthermore, Cr is common in mining areas while Hg comes with coal burning, and Zn and Cu come with the incineration of biomass [24, 25]. The PM size forming complex with the TM is also an important factor since finer metal-particulate complexes of less than PM 2.5 μm (≤PM2.5) are known to have more health hazards [26]. There could be direct consequences of TMs in the air like faster infrastructural decay, acidification of rain, and formation of smooth [27]. The time of assessment of TM in the atmosphere is important since there had been a dynamic shift in the metal composition of air today relative to 30 years ago [28].

1.1.1 Ecosystem and its intricate dependent on the environment: redox implications along the trough

An ecosystem describes a community of living (biotic) and non-living (abiotic) things interacting with each other in a dynamic and evolving environment (Figure 2). Over time, the equilibrium of survival forces tends to shape the environment, as a result of conquest for nutrition and the pressure of population growth [29]. Considering the fact that different states of the environment can serve as an ecosystem of their own, contamination of the environment may be seen as contamination of different ecosystems since boundaries may or may not exist [30]. The ecosystem is valuable to man because of the economic and possible esthetic values. The functional system of an ecosystem involves activities of different organisms, their different life processes ranging from production, consumption, and excretion, and how all these affect the environment [30]. Humans benefit as a major source of food, fuel, and fiber, as natural cycling of both water and gases. The distortion of an ecosystem by man is assuming a catastrophic dimension by altering the land for his purposes and over-harvesting biological resources like forest damage and excessive fishing [31]. Estimates have it that man uses up to 40% of the ecosystem for economic ventures which has altered the ecosystems leading to the extinction of species, replacement of high biological diversities with lower ones, and ecosystem contamination [32]. These distortions will result in reduced ecosystem biomass as a result of alteration in the process of converting solar radiation to chemical energy; the first trough in the energy matrix [33].

Figure 2.

Schematic representation of the relationship between biotic and abiotic components of an ecosystem and how they relate to each.

Pollution of ecosystems with TM has generated a lot of environmental concern and comes with severe global health implications. Some TMs that plants and micro-organisms require will enhance the growth of such an ecosystem so long as the concentration is not up to the threshold that elicits toxicity. TMs in the environment do not last forever as mono-metals but undergo several chemical processes which will result in the modification of their bioavailability and mobility within different compartments [9]. Such chemical processes include: 1. Complexation; 2. Desorption; 3. Adsorption; 4. Dissolution; and 5. Precipitation. The first sufferer in terms of TM ecosystem contamination is the soil micro-organisms [34]. TMs induce these damages by either direct intoxication of biotic producers (plants) or altering the physiological and biochemical properties of micro-organisms resulting in a reduction in soil arability. TMs like Cr, Cd, and even high levels of Zn are known for such, possibly via the generation of oxidative stress [35]. These metals affect not only microbial growth but also alter genetic variation, morphology, and metabolism. Proteins are denatured, cell membranes peroxidized, and enzymes and DNA distorted leading to altered decomposition capacity and reduced nutrients for plant growth [34]. TMs could attack plants directly destroying their cell membranes and subsequently chlorophyll, resulting in decreased photosynthetic activity and plant growth. Either by attacking plants directly or indirectly via distortion of the soil micro-organism community, TMs result in a decrease in plant production. Because plants are the first in the trophic level, any decrease in plant availability for nutrition will affect plant-dependent herbivores [36]. The catastrophic consequences of altering a plant’s biodiversity start with damage to photosynthesis-dependent cascades. In addition to TMs damage to chloroplast membrane, there could be damage to essential enzymes involved in photosynthesis. This results in inability of plants to generate enough energy (sugars and starch) since it loses the ability to convert CO₂ and H₂O from air and soil to give O₂ and glucose (electron transport process). Thus, plants are at the heart of CO₂ sink and O2 generation that the consumers and decomposers depend on (Figure 3) [37].

Figure 3.

Schematic representation of the interactive effect between sunlight, carbon dioxide water, and plant during photosynthesis to generate sugar and oxygen.

The catastrophic consequences of dysregulation of the balance between CO₂ and O₂ will be the termination of all respiratory-dependent species, including man [38]. Green plants are endowed with innate repair mechanisms to keep a natural balance in check. However, it is worth mentioning that some TMs participate at one point or another in the photosynthetic process. Metals like Fe, Cu, and Mn serve as co-enzyme in the photosynthetic process since they serve as cofactors of metalloproteins during the electron chain process in photosynthesis. The concentration of metals needed is minute, and any slight increase beyond this amount becomes deleterious and damaging to the ecosystem’s redox balance [39]. Following the disruption of the plant’s energy process, all other living things higher in energy trough suffers deprivation. There will be decreased species diversity and abundance, leading to a shortfall in the quality and quantity of nutrients for herbivorous animals [40]. Animals from higher troughs will suffer a similar fate, scampering for food with higher-than-usual competition and adaptation for survival. Man too will have less nutrition to depend on, increasing their propensity for diseases, with decreased immunity, poor growth, and development [41]. Also, the disruption of the ecosystem by TM affects both biotic and abiotic-dependent processes. Animals like birds that use trees as shelter will become excessively exposed to both predators and environmental conditions that may be inimical to their survival. Some of the abiotic factors that have a symbiotic balance with plants like soil will be exposed to excessive erosion and there may be dysregulation of the climate and environment [42]. Another major issue with TMs exposure to plants is that of absorption by plants, passing it up along the energy chain with possibility of bioconcentration and biomagnification of these metals. Higher animals, including man that depends on these plants or other animals indirectly consume more TMs than lower animals (Figure 4).

Figure 4.

Schematic representation of different energy levels in an ecosystem and how trace metals can become concentrated and magnified along the chain.

The consequences of TMs on higher animals cannot easily be quantified. Most TMs like Cd, As, Pb, etc. are multi-organ toxicants; affecting every part of the body [43]. Organ damages lead to decreased morbidity and mortality, and the effect on the gonads particularly will lead to decreased population and congenital abnormalities [44]. Ultimately, all these toxicological milieus will lead to further distortion of the ecosystem.

1.1.2 Acceptable limit of trace metals in the environment (ecosystem)

Due to the deleterious nature of TMs, acceptable limits in the environment had been set to forestall decreased mortality arising from accidental consumption. Of particular health importance is the preponderance of TMs to induce carcinogenicity. Studies on the occupational effect of exposure in humans and long term animal studies had been used to classify TMs based on their carcinogenic risk by the International Agency for Research on Cancer (IARC) (Table 1). This represents the first and primary step in carcinogenic risk assessment.

Groups	Criteria
Group I	Agent is carcinogenic to humans
Group 2A	Agent is probably carcinogenic to humans
Group 2B	Agent is possibly carcinogenic to humans
Group 3	Agent is not classifiable as to its carcinogenicity to humans
Group 4	Agent is probably not carcinogenic to humans

Table 1.

Criteria for assessment of the carcinogenicity of a chemical (TMs).

The second step in the assessment of chemicals including TMs involves establishment of the threshold for toxicity to manifest. A tolerable daily intake (TDI) gives an idea of daily exposure via the ecosystem that can manifest in toxicity using a sensitive end-point.

$$\mathrm{TDI}=\frac{\text{NOAEL or LOAEL or BMDL}}{\mathrm{UF}\text{and}/\text{orCSAF}}$$

where NOAEL—no observed adverse effect level; LOAEL—lowest observed adverse effect level; BMDL—lower confidence limit on the benchmark dose; UF—uncertainty factor; CSAF—chemical specific adjustment factor.

The guideline value can be derived from the TDI based on the formula;

$$\mathrm{GV}=\frac{\mathrm{TDI}\times \mathrm{bw}\times P}{C}$$

where bw—body weight; P—fraction of TDI allocated to that ecosystem; C—daily consumption of either food or water from that ecosystem.

World Health Organization (WHO) had set guidelines for permissible levels of some TMs in water which can guide the levels in an ecosystem (Table 2).

Trace metal	Guideline value (mg/l)
Selenium	0.01
Nickel	0.07
Molybdenum	0.07
Mercury	0.006
Manganese	0.4
Lead	0.01
Chromium	0.05
Copper	2
Cadmium	0.003
Barium	0.7
Arsenic	0.01

Table 2.

Values of TMs as guidelines from WHO.

1.2 Mechanism of trace metal’s alteration of the ecosystem redox balance

TMs are believed to have a similar but complex mechanism of action in carrying out whatever toxicity that is associated with it. In living organisms, some of these metals are the fulcrum of homeostasis which involves oxygen-hypoxia sensing and therefore contribute to the intricate processes of metal absorption and storage. This homeostatic function is under strict control, but any imbalance leads to the activation of other biochemical pathways like the Haber Weiss/Fenton reaction pathway. This will lead to a generation of reactive oxygen species (ROS) and reactive nitrogen species (RNS) [43, 45]. Some TMs like Cd, As, Pb, etc. that do not participate in biological reactions also generate ROS and RNS indirectly, possibly by stimulating nicotinamide adenine dinucleotide phosphate oxidases (NADPH oxidases), or by competing for the metal binding site of an enzyme or protein and taken over the active site, or by attacking the sulfhydryl moiety of proteins [46]. ROS and RNS are not entirely a nuisance in cell homeostasis as they play a role in the growth of micro-organisms, cell cycle and stress response, defense, cell signaling, and apoptosis [47]. These metals indirectly generate ROS and RNS also has the potential to displace metals like Fe, Cu, Co, etc. from their active sites, making them available for catalysis, which can result in the further formation of ROS and RNS (Figure 5) [48]. Living things are endowed with an efficient system for removing excess ROS and RNS in their cells to avoid injury. There is an efficient antioxidant system that is innate in all living organisms for stress control. Most cells possess stress-sensing techniques that ring a bell once the oxidative and nitrative stress levels go beyond a threshold [49]. Glutathione is the first line of defense in this regard having the ability to neutralize most free radical species like lipid peroxides, peroxynitrites, hydroperoxides, superoxide, nitric oxide, and carbon radicals resulting in the protection of essential body parts [50]. Furthermore, there are other enzymatic and non-enzymatic components of the antioxidant armamentarium available to living organisms for protection. Non-enzymatic antioxidants include vitamins C and E, polyphenols, carotenoids, flavonoids, etc. that can donate electrons and neutralize free radicals, thereby preventing pathological injury [51]. Enzymatic antioxidants, on the other hand, include superoxide dismutase (SOD) which causes the dismutation of superoxide radical to produce oxygen and hydrogen peroxide (Figure 5), and catalase which catalyzes the decomposition of hydrogen peroxide to water and oxygen. By removing peroxide radicals, these two enzymes work in tandem to keep ROS from going beyond optimal level [52]. Some enzymes are involved in maintaining the level of glutathione in living organisms.

Figure 5.

Schematic representation showing the generation of reactive oxygen species (ROS) by trace metals via the formation of superoxide radicals. MPO is myeloperoxidase and SOD is superoxide dismutase.

Glutathione exists in both reduced and oxidized forms with the reduced form being more in amount. The reduced form (GSH) can convert hydrogen peroxide (ROS) to water in a reaction catalyzed by glutathione peroxidase (GPx) while in itself becoming oxidized (GSSG) [53]. GSSG can become reduced back to GSH by glutathione reductase (GR), thereby regenerating GS to participate in another round of reaction (Figure 6). There is always a balance between the pro-oxidant forces and the antioxidant forces for the optimal health of living organisms in any ecosystem. Where the pro-oxidant forces dominate, oxidative stress ensues with its consequential damages. By increasing the prooxidant forces and creating redox imbalance, TMs compromise the health of the ecosystem from the producers (plants) to the consumers. If this redox imbalance is unchecked, the world as a global ecosystem will be in peril [43, 54]. This redox imbalance will cause the activation of adaptive cellular responses in the organisms along the food chain. Plants will increase the expression of genes that will support both extracellular and intracellular sequestration. Organic anions like malate, oxalate, etc. will lead in the extracellular sequestration while polymers like pectin, cellulose, lignin, and hemicellulose lead the internal.

Figure 6.

Schematic diagram showing the conversion of glutathione (GSH) from the reduced form to the oxidized form (GSSG) by glutathione peroxidase (GPx) and the regeneration back to the reduced form by glutathione reductase (GR). GSH could also get oxidized by glutathione oxidase.

In the animal kingdom, activation of the adaptive cellular mechanisms leads to interference with immune homeostasis resulting in inflammation. Pro-inflammatory cytokines and chemokines like nuclear factor kappa B (NF-κB), tissue necrosis factor (TNF), interleukins 1B, 6, 8, etc. (IL-1B, IL-6, IL-8) get activated [55]. Activation of the inflammatory pathways will also lead to other cascades of activations like the cell death pathways. There will be an increase in the expression of genes mediating apoptotic pathways like caspase 3, 8, 9, and 10 resulting summarily in death and damage to the ecosystem [56].

1.3 Remediation and restoration of the ecological redox imbalance

Bioremediation is the scientific approach usually used to remove and or convert damaging environmental contaminants like TM into less harmful ones. It involves physical, chemical, or biological processing like adsorption, precipitation, ion exchange, electro-dialysis, complexation, electrostatic attraction, redox process, etc. [57]. It is an eco-friendly, effective, and cost-effective technique for the treatment of soil and water contaminated with unwanted and hazardous chemicals [58]. Ion exchange has recorded some level of success as it can remove TMs even at low concentrations. The major setback to its use is the high cost associated with it and the fact that pH usually affects its efficiency [59, 60]. Recently, interest in the use of adsorption has been on the increase because of the low cost involved. Nanomaterials, industrial biowastes, metal organic frameworks (MOF), microbes and nanocomposites are being used for adsorption purposes [61]. Precipitation is ideal, especially in TM-contaminated effluent-like water. It is cost-effective and requires fewer technicalities than ion exchange and the precipitate comes out as carbonates, hydroxides, and sulfides which are removed by sedimentation and filtration [62]. Electrodialysis (ED) is a promising and emerging technique for removing and recovering TMs from mixtures and matrices. Its major merit is that it can be combined with other methods for improved efficiency [63]. Complexation involves establishing a coordination complex between macro ligands and coordinating atoms of TMs in other to increase their size and molecular weight. It is ideal for the removal of TMs in industrial setups like paper mills, textiles, pulp, water treatment, agriculture, etc. with moderate cost [64]. Recently, attention regarding TMs removal from contaminated water has shifted to the use of electrically charged ions for attraction. This involves the use of materials that attract TMs ions to adsorb and remove it from the contaminating environment [65]. A relatively new trend in the removal of TMs involves the redox process which is the redox technique. So many other bioremediation processes involve redox reactions such as electrokinetics, the use of nanotechnology, ultrasonication, etc. Biological techniques in bioremediation use mainly organisms like fungi, bacteria, plants, or plant parts to degrade, reduce, remove or recover TMs in soil and water [66]. Use of microbes in bioremediation could be by bioaugmentation, bioventing, bio-sparging, land farming, bio-stimulation, bio-piling, or composting. Bio-augmentation involves the use of organisms to speed up the rate of degradation of a TM. This requires information on the diversity of micro-organism present before the introduction of additional organisms [67]. In bioventing, there is increased aeration of contaminated water or soil to promote increased bioactivity of the indigenous micro-organisms as a way of metabolizing TM [68]. In bio-sparging, oxygen is injected and made to become saturated in the contaminated area to aid biodegradation and bio-transformation [69]. Furthermore, land farming involves the mixing of contaminated soil with soil amendment substances like nutrients and bulking agents and tilling back into the soil with occasional tilling to aid aeration [70]. Bio-stimulation is an ideal technique for water contaminated with TM and involves supplying the contaminated water with growth-limiting nutrients like phosphorus and nitrogen as a way of facilitating the interaction of micro-organisms in the fluid [71]. The technology of bio-piling encompasses mixing excavated soil with soil amendment that is in compost piles and enclosed for decontamination [72]. Compost bioremediation of TM-infested areas involves a process where both fungi and bacteria are used to break down these contaminants in water and soil [73]. The bottom line in all these biological techniques is the use of organisms that can metabolically use these TMs as an energy source while converting it to less toxic forms [74]. Proper bioremediation is the first step in bio-restoration of TM dysregulated redox imbalance in a contaminated environment.

2. Conclusion

TMs contamination of the environment is of global dimension with its associated risk in terms of threat to biotic and abiotic components of the environment. These TMs are naturally found in the crusts of the earth but contaminate the environment following anthropological activities. Some TM can be found in some food, where minute quantities could aid the normal homeostatic functions of living organisms. In large amounts, they cause potential damage to the ecosystem that supports life, including that of man. Scientists believe that the unifying mechanism of environmental distortion is the formation of free radicals which cause damage via chemical electron abstraction. Bioremediation of soil and water contaminated with TMs has offered some relief in terms of mitigation and holds promise for a balanced redox ecosystem.

Conflict of interest

No conflict of interest to declare.