Abstract
Accumulation of heavy metals especially cobalt (Co) in agricultural fields and water bodies due to natural as well as anthropogenic factors is major concern. Although it is an important constituent of vitamin B12, yet its higher exposure produces significant ramifications in crop plants. It affects biomass and concomitantly reduces crop yield that in turn causes substantial financial loss to farmers. To counter this heavy metal toxicity, the plants have devised mechanisms either to detoxify or accumulate the contaminants. Further, there are various bioremediation strategies that can be used to get rid of Co from the given medium. Phytostabilisation, phytoextraction, rhizofiltration are some of the techniques used worldwide to reduce cobalt in the fields. This review emphasis upon the uptake, transportation, accumulation of cobalt in plants and discusses the remedial strategies available presently to effectively remove it from mediums like soil and water bodies.
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1 Introduction
Heavy metals (HMs) are the naturally occurring metal elements having atomic number > 20 with characteristically high atomic density (4 g/cm3 or five times than that of H2O), and may be toxic at very low concentrations [1, 2]. Their accumulation in soil is regarded as one of the major culprits for degradation of pedosphere. In nature, HMs are present deeply hidden in the earth as a non-degradable constituent of the earth’s crust [3]. But overexploitation of natural resources has given an easy way to these HMs to rise up to the surface of earth. These are present in soil either innately (volcanic activities, weathering of rocks) or added to it by various anthropogenic activities like metal smelting, overuse of fertilizers and industrial waste etc. [4]. Further, it has been found that anthropogenic mediated addition of HMs in atmosphere is almost three times higher as compared to the natural factors [5]. They are discharged in soil and water bodies either in solution or solid forms. In water bodies, they get built up on the sea floor or get adsorbed on to the solid objects [6]. Likewise in soil, HMs keep on piling up because they do not get oxidized by microbes unlikely organic contaminants, hence continue to persist in the soil for long duration of time [7]. They even obstruct the degradation of organic contaminants by inhibiting microbial activity [8]. From soil they slowly leach into underground water to contaminate the water table. The exposure of soil fauna to HMs disturbs their distribution and hence reduces fertility of soil [9]. HMs are known to reduce the growth of sulphate reducing bacteria by denaturing their proteins and inactivating enzymes [10]. Plants growing at such contaminated sites take up these HMs from affected soil–water, and keep on accumulating these HMs. This pile up of HMs in plants gets magnified along the linear network of food chains which may affect human health [11]. Owing to their non-biodegradable nature and longer biological half-life, HMs are more toxic than most other xenobiotics [12]. To break the burgeoning HM concentrations via food chain, it is necessary to remediate the soil which acts as a sink from where autotrophs start biomagnification (Fig. 1).
HMs (Ni, Cr, Fe, Zn, Mn and Co) at low concentrations play an essential role in the growth and development of plants but at concentrations higher than certain threshold levels cause toxicity to the plants [13,14,15]. Pertaining to their toxic nature, HMs are slurred as severe pollutants [10]. Their toxicity in plants depends upon a number of factors like plant species, form in which metal is present in the soil, soil type, and pH of the soil etc. [1]. Amongst all the HMs, only a few are essential for the survival of both plants and animals, and that too are required in very low amounts (Table 1). An exposure greater than their permissible limits, leads to cellular and subcellular damage (damage to membranes, mitochondria, chloroplast) due to altered plant metabolism [16]. The HMs manoeuvres various strategies to exert damage at cellular levels. Attributing to their high redox activities and rich coordination chemistry, HMs manage to escape the cellular control checkpoints (homeostasis, compartmentalization, transportation etc.) to bind various subcellular targets that are vital for cell survival. These escaped HMs bring about oxidative damage to biological macromolecules [17]. The most common way of persuading cellular damage by HMs is by inducing oxidative stress by alleviating free radical levels [18]. Reactive oxygen species (ROS) are generated either directly or indirectly by activating ROS generating enzymes [19]. Depending upon ROS generating potential, the bioactive metals are categorized into two classes, i.e. redox active and non-redox active metals (Fig. 2). The Redox active metals (Co, Cr, Mn, Fe, Cu) are those that can damage cells by directly generating ROS by up-regulating Haber–Weiss and Fenton reactions [17, 20]. The non-redox active metals are metals (Cd, Ni, Hg, Zn and Al) that damage the cells and their subcellular vitals by indirectly accruing ROS level via glutathione depletion, inhibiting antioxidant enzymes, binding active sulfhydryl groups of proteins and activating ROS producing enzymes such as NADPH oxidase [17, 20, 21]. This review deals with uptake, accumulation, transport, toxicity and remediating strategies of cobalt from contaminated soils and water bodies.
Cobalt (Co) was discovered by Georg Brandt in 1735 [22, 23]. It is a heavy metal having atomic number 27 and atomic mass 58.93 amu. Co is required as a trace element in both plants and animals. Co exists in numerous inorganic complexes with different oxidation states, but the most common states are + 2 and + 3, respectively [24]. Co is a beneficial element for leguminous plants for the growth, metabolism, and development of root nodules [25]. Its importance to the rest of the plant species is still equivocal. It plays an important role in the activities of various enzymes and coenzymes like vitamin B12 (cyanocobalamin) [26]. The approximated consumption of Co by humans from food is 5–40 µg/day [27,28,29] Tolerable limit of Co in soil for the growth of plants was found to be 0.2–0.5 ppm [30]. Some plant species are able to grow in soil possessing high concentrations of Co up to 4000–10,000 ppm. Co acts as a coenzyme in a number of cellular processes like the fatty acid oxidation and synthesis of DNA. It was found that deficiency of Co in grasses and feedstuffs leads to diseases in ruminants, like scaly skin, loss of appetite, anaemia and bone fragility [31, 32]. Toxic concentrations of Co inhibit active transport in plants. Relatively higher concentrations of Co have toxic effects, including leaf fall, inhibition of greening, discoloured veins, premature leaf closure and reduced shoot weight [33]. High concentration of Co leads to numerous dysfunctions in the plant system. These mainly include production of reactive oxygen species (ROS), hydroxyl radical (˙OH) generation, formation of hydrogen peroxide (H2O2) radicals, increased MDA, proline content and alteration of antioxidant enzyme activities [34, 35]. ROS generation under Co stress in plants generally causes disturbance in photosystem II and stimulates disruption in electron transport chain [36]. Increased Co content in the soil also reduces photosynthetic pigments and nitrogen metabolism in the plants [37]. Thus, there is a strong need to remediate Co accumulated sites.
The distribution of cobalt is species dependent. Generally leguminous plants contain more Co as compared to grasses and grain crops [38, 39]. Toxic concentrations of cobalt inhibit active transport in plants. Also application of excess of Co has detrimental effects on plant growth and metabolic functions, including leaf necrosis and interveinal chlorosis, inhibition of cellular mitosis and chromosomal damage [40]. Co is also known to inhibit seed germination, root and hypocotyl elongation [41]. Co appears to be toxic when uptake of essential elements like iron and calcium are inhibited [42, 43].
2 Natural source of cobalt
Cobalt is well known to be siderophile, lithophile as well as chalcophile element [44]. In nature, it is found along with iron, nickel, silver, lead, copper, manganese and also found to exist as carbonates [45]. It also exists in the form of minerals like cobaltite, skutterudite, erythrite, spherocobaltite and heterogenite. It is found abundantly in both sedimentary and igneous rocks. Its average abundance in earth’s crust quite low as compared to other HMs, i.e. 25–30 mg/kg that is higher only to scandium. The ultramafic rocks have higher abundance of Co, i.e. 100 mg/kg. During differentiation of crust from balastic magma, most of the Co combines with ferromagnesian minerals, which is further limited by the number of lattice sites in Fe–Mg. In granite rocks, Co forms tight coherence with magnesium. In open ocean, the Co is present in concentration of about 40 pmol/kg. It has very little mobility [45,46,47].
3 Anthropogenic source of cobalt
About 15% of the total Co produced worldwide is used for handling and manufacturing of hard metals [48]. Cemented carbide contains 5–30% of cobalt. Cement industries and carbide tool grinding plants are also responsible for Co leaching [49, 50]. Industries related to e-waste processing have also been found to release Co above legal threshold levels [51, 52]. Polishing disc used in diamond polishing is also made up of fine cobalt. It is also a potential source of generating Co dust [53, 54]. Pigment and paint industries also use Co as siccative that speeds up the process of drying [55]. Incinerators produce bottom ash which contains Co that leaches to the soil and ground water [56]. Due to mining activities, Co concentration in surrounding soil and water bodies elevates way beyond regional background levels [57]. Mobile batteries, televisions (TVs), liquid crystal display TVs, and computer monitors also contain Co and become potential source of Co contamination [58,59,60]. Several cosmetic products are also source of Co as impurities [61]. Many dietary items like chocolate, butter, fish, etc. also contain Co and become source of Co contamination [28, 62, 63]. Many older medicinal practices use Co preparations to treat anaemia, post-menopausal symptoms in women [64,65,66].
4 Cobalt uptake, accumulation, transport in plants
Co is a micronutrient which can be accumulated by plants in very less amount. Co ions may get accrued in the plant parts like fruit, grains and seeds. It is essential to all animals and microorganisms [67]. However, a physiological requirement for Co has not been demonstrated in higher plants. Co is emitted to the atmosphere in small quantities through activities like coal combustion and mining, processing of Co containing ores, and the production and use of chemicals/fertilizers containing Co salts. Although concentration of Co in plants is normally 0.05–5 mg/kg dry weight, but this value goes up to 111–245 mg/kg in plants grown in mining area [68]. Metal ions do not biodegrade. Thus the removal of excess metal ions from polluted sites and their secure sequestration are important for the production of safe food, and viable environment [69]. Uptake, transport and distribution of Co are species dependent and are governed by various mechanistics [70, 71]. Transport proteins and intracellular affinity binding sites mediate the uptake of Co ions across the plasma membrane. Many classes of proteins have been entailed in heavy metal transport in plants [72]. These include CPx-type ATPases that are involved in the overall metal-ion homeostasis and tolerance in plants, the natural resistance-associated macrophage protein (Nramp), and the cation diffusion facilitator (CDF) family proteins, zinc–iron permease (ZIP) family proteins, etc. [73]. Arabidopsis thaliana Heavy Metal Associated 3 (AtHMA3) protein belonging to the P-type ATPase family, has been found to be involved in heavy metal transport [74]. They demonstrated AtHMA3 is located in the vacuolar membrane of plant. They also found that AtHMA3 improved plant tolerance to Cd, Co, Pb, and Zn. Studies have demonstrated involvement of CPX motif in Co ion coordination during transport [75] Moreover, the metal specificity of these ATPases remains unclear. Studies on Synechocystis sp. have shown that a knockout of the encoding ATPases gene leads to increased levels of intracellular Co2+ and reduced Co2+ tolerance [76]. It has also been reported that in higher plants Co ions get bind with the roots, and transferred in the body via passive transport. Co ions enter into the cell through plasma membrane and may be translocated to the whole plant with the help of IRT1 transporters [77].
5 Toxicity of cobalt in plants
Due to foolhardy use of fertilizers, wastewater discharge, coal and motor fuel combustion processes, increased mining of the cobalt ore, the concentration of naturally occurring Co has increased [78]. Cobalt is not relegated as an essential element for plants. Nevertheless, it is usually distinguished as a beneficial element having role in certain biochemical and physiological processes of plants. Higher levels of Co in soil causes toxic impacts on plants that are reflected in their morphology as well as physiology [79,80,81] (Table 2).
Studies also suggested that Co ions effect the growth of Lemna minor with increase in concentration [82]. Chatterjee and Chatterjee [83] reported that excess Co led to the occurrence of iron (Fe) deficiency in young leaves. Higher Co concentration reduced the biomass, chlorophyll content, and catalase activity, while increased the activities of peroxidase, acid phosphatase, ribonuclease enzymes, and carbohydrate, phosphorus fractions in leaves. Co reduces the translocation of P, S and Cu and drops the transpiration rate and water potential in the leaves of cauliflower [1]. Application of 5 mM Co resulted in reduction in seedling growth due to chlorosis of the younger leaves [84]. Higher concentrations (10−2 M) of Cr, Co induced reduction in seed germination rate and radicle growth, while lower concentrations (10−6–10−4 M) raised sugar and chlorophyll contents [85].
Effect of Co2+, Ni2+ and Cd2+ on growth and metabolic parameters in cabbage produced visible symptoms like chlorosis. Co2+ treated plants showed purple colouration along leaf margins. Equimolar concentrations of Cd2+ and Ni2+ inhibited growth of plants causing severe symptoms of toxicity. Excess concentrations of the three metals lead to decrease in chlorophyll content, uptake and translocation of Fe in leaves and reduced proline activity [86]. The cobalt toxicity on growth and metabolism of tomato plants was studied in sand medium at five levels of concentration, i.e. 0, 0.05, 0.1, 0.4 and 0.5 mM. Strong effects of cobalt on tomato were observed at 0.5 mM after 3 days of metal supply. The prominent symptoms were appearance of chlorosis on young leaves followed by necrosis and withering. Supererogatory levels of Co significantly affected biomass, concentrations of various minerals like P, S and Fe, and diminished level of chlorophyll a and b, DNA, starch as well as reducing and non-reducing sugar levels. Increased concentrations of metal also inhibited the activity of antioxidative enzymes like catalase, peroxidase, ribonuclease and acid phosphatase [87]. Binary effect Co with (0, 20 and 40 mg/kg soil) and Ni with (0, 25 and 50 mg/kg) was studied on growth, yield, content of micro- and macronutrients and anthocyanins of Hibiscus sabdariffa L. The results revealed that Co and Ni in combination of 20 + 25 mg/kg−1 significantly increased plant height, number of branches as well as dry and fresh weights. The lower doses of Co showed synergistic effect on Ni, Mn, Zn and Cu [88].
Some studies reported that increased concentration (10, 50, 100, 150 mM) of heavy metals (Ni, Co, Fe) decreased the rate of seed germination, root length, shoot length, protein and phenolics content in broad beans (Vicia faba L.). The metal toxicities of various metals studied were found in the order Co > Ni > Fe. The workers also inferred that bean is a metal resistant plant which has contrived various mechanisms such as denovo synthesis of anti-stress protein or mitigation of ROS by enhanced phenolic production to combat metal stress [89]. The phytoremediating ability of Eleusine indica (grass) was studied in Cu, Cd, Cr, Co and Pb laden soils. The preliminary levels of Cu, Cd, Cr, Co and Pb in soil, root and shoot of the grass were: soils: 104.5, 5.1, 36.4, 13.3, 14.4 μg/g; root: 164.2, 4.3, 153.9, 11.5 and 24.7 μg/g and shoot of the grass were: 111.5, 2.9, 51.2, 11.1, and 60.7 μg/g, respectively. Enrichment coefficient (EC) and translocation factor (TF) were calculated to estimate the phytoextraction ability of E. indica. They found that Cu, Cr and Pb had the highest EC of 1.07, 1.41 and 4.22, respectively [90].
The possible mechanism of actions of cobalt in plants, and proposed way of action of oxidizing and chelating agents is presented in Figs. 3 and 4.
6 Bioremediation strategies
Bioremediation is an innovative and inventive biological approach that explores potential of microorganisms and plants to reduce and remediate soil and water bodies from toxic chemicals [91, 92]. Bioremediation explores potential of microorganisms to remediate given medium viz., Bacillus spp. and Pseudomonas aeruginosa are used to remove Zn and Cu [93].
6.1 Phytoremediation
Phytoremediation is the direct use of green plants and their associated microorganisms to decrease or stabilize pollution in soils, sediments, ground water, surface water and sludge [94]. Here, metal tolerant and hyper-accumulating plant–microbe interactions are also explored for mobilization of metals [95, 96]. First used in 1990, it is a natural process used to remediate the contaminants, and has gained a lot of consideration during the last few years, on account of its being cost effective and promising technique [97]. A number of phytoremediation techniques are available, but in the following section only those are discussed which are involved in remediation of Co.
6.1.1 Phytostabilization
It is method of establishment of metal tolerant vegetation cover over contaminated area in order to immobilise contaminants within rhizosphere zone of plant. Growth of vegetation on contaminated area restricts dispersion of metal laden soil particles by air or water. Further, the microbes growing in rhizosphere immobilize the contaminants by precipitation or adsorption mechanism [98, 99]. Moreover, retention or immobilisation of HMs in soil is also dependent upon pH of soil as most of the adsorption sites are pH dependent. An inverse relationship between increase in pH (from acidic to alkaline) and leaching of Co was observed where, increasing pH value from 1 to 3, leaching of Co was significantly decreased up to 30%. This showed that Co is weakly bound in mineral phase as compared to other HMs [100].
6.1.2 Phytoextraction
It involves the removal of contaminants from soil or water body through roots of plants and their accumulation in shoot system. Thus, contaminant is removed from the medium [101]. This technique is usually employed when phytostabilization is not possible. The success of phytoextraction is dependent upon two factors, i.e. biomass production (where metal is stored) and metal bioconcentration factor (ratio of contaminant in shoot by its concentration in medium). There are more than four hundred plants which are reported as hyperaccumulators. A study by Malik et al. [102] presented Alysssum murale as potential hyperaccumulator of Co. A. murale accumulated sixty times more Co, i.e. 1320 mg Co/kg dry weight as compared to Brassica juncea in Co enriched soil. Thlapsi caerulescens is another hyperaccumulator of Zn also used for phytoextraction of Co. Lycopersicon esculentum was also shown to act as accumulator of Co with accumulating Co in all above ground plant parts except flowers and fruits [103].
6.1.3 Rhizofiltration
It is the technique exclusive used in water bodies. It explores potential of plant roots to take up and get rid of contaminants from water body [104]. The contaminants are absorbed and precipitated in the roots from medium. The plants are first raised hydroponically and then they are transferred to the given contaminated water body [105]. Epipremnum is successfully used for rhizofiltration of Co. Plant showed a bioconcentration factor of 10.69 for Co [106]. Prajapati et al. [107] have effectively used Pistia stratiotes in their experimental set up to remove Co from water medium.
7 Conclusion
Increased contamination of cobalt in the agricultural fields and water bodies is alarming. A number of remedial procedures are available to remediate our contaminated sites. But the interaction of metals sometimes, makes one or other metal immobile that limits use of bioremediation strategies. So, new techniques and strategies should be continuously devised to reduce limitations of bioremediation procedures.
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Authors are thankful to University Grants Commission, New Delhi for research fellowship granted (vide Grant No. F.14-2(SC)/2010(SA-III) to the first author Sonia.
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Mahey, S., Kumar, R., Sharma, M. et al. A critical review on toxicity of cobalt and its bioremediation strategies. SN Appl. Sci. 2, 1279 (2020). https://doi.org/10.1007/s42452-020-3020-9
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DOI: https://doi.org/10.1007/s42452-020-3020-9