1. Introduction
With the growth of industry, there has been a considerable increase in the discharge of industrial waste to the environment, chiefly soil and water, which has led to the accumulation of heavy metals, especially in urban areas. Slow depletion of heavy metals also takes place through leaching, plant uptake, erosion and deflation. The indiscriminate release of heavy metals into the soil and waters is a major health concern worldwide, as they cannot be broken down to non-toxic forms and therefore have long-lasting effects on the ecosystem. Many of them are toxic even at very low concentrations; arsenic, cadmium, chromium, copper, lead, mercury, nickel, selenium, silver, zinc
etc. are not only cytotoxic but also carcinogenic and mutagenic in nature [
1]. Some metals are required by plants in very small amounts for their growth and optimum performance. However, the increasing concentration of several metals in soil and waters due to industrial revolution has created an alarming situation for human life and aquatic biota. This is evident from various reports citing harmful effects of heavy metals on human health (
Table 1).
In order to make the environment healthier for human beings, contaminated water bodies and land need to be rectified to make them free from heavy metals and trace elements. There are several techniques to remove these heavy metals, including chemical precipitation, oxidation or reduction, filtration, ion-exchange, reverse osmosis, membrane technology, evaporation and electrochemical treatment. But most of these techniques become ineffective when the concentrations of heavy metals are less than 100 mg/L [
2]. Most heavy metal salts are water-soluble and get dissolved in wastewater, which means they cannot be separated by physical separation methods [
3]. Additionally, physico-chemical methods are ineffective or expensive when the concentration of heavy metals is very low. Alternately, biological methods like biosorption and/or bioaccumulation for removal of heavy metals may be an attractive alternative to physico-chemical methods [
4]. Use of microorganisms and plants for remediation purposes is thus a possible solution for heavy metal pollution since it includes sustainable remediation technologies to rectify and re-establish the natural condition of soil. However, introduction of heavy metals into the soil causes considerable modification of the microbial community, despite their vital importance for the growth of microorganisms at relatively low concentrations [
5]. The modification of the microbial make up is mainly brought about by exerting an inhibitory action through blockage of essential functional groups, displacement of essential metal ions or modification of active conformations of biological molecules [
6,
7]. The response of microbial communities to heavy metals depends on the concentration and availability of heavy metals and is a complex process which is controlled by multiple factors, such as type of metal, the nature of the medium, and microbial species [
8].
Table 1.
Toxic effect of some heavy metals on human health.
Table 1.
Toxic effect of some heavy metals on human health.
Heavy Metal | EPA Regulatory Limit (ppm) [9] | Toxic Effects | Ref. |
---|
Ag | 0.10 | Exposure may cause skin and other body tissues to turn gray or blue-gray, breathing problems, lung and throat irritation and stomach pain. | [10] |
As | 0.01 | Affects essential cellular processes such asoxidative phosphorylation and ATP synthesis | [11] |
Ba | 2.0 | Cause cardiac arrhythmias, respiratory failure, gastrointestinal dysfunction, muscle twitching and elevated blood pressure | [12] |
Cd | 5.0 | Carcinogenic, mutagenic, endocrine disruptor, lung damage and fragile bones, affects calcium regulation in biological systems | [1,13] |
Cr | 0.1 | Hair loss | [1] |
Cu | 1.3 | Brain and kidney damage, elevated levels result in liver cirrhosis and chronic anemia, stomach and intestine irritation | [1,14] |
Hg | 2.0 | Autoimmune diseases, depression, drowsiness, fatigue, hair loss, insomnia, loss of memory, restlessness, disturbance of vision, tremors, temper outbursts, brain damage, lung and kidney failure | [15,16,17] |
Ni | 0.2 (WHO permissible limit) | Allergic skin diseases such as itching, cancer of the lungs, nose, sinuses, throat through continuous inhalation, immunotoxic, neurotoxic, genotoxic, affects fertility, hair loss | [1,18,19,20] |
Pb | 15 | Excess exposure in children causes impaired development, reduced intelligence, short-term memory loss, disabilities in learning and coordination problems, risk of cardiovascular disease | [1,14,21] |
Se | 50 | Dietary exposure of around 300 µg/day affects endocrine function, impairment of natural killer cells activity, hepatotoxicity and gastrointestinal disturbaces | [22] |
Zn | 0.5 | Dizziness, fatigue etc. | [23] |
Bioremediation is an innovative and promising technology available for removal of heavy metals and recovery of the heavy metals in polluted water and lands. Since microorganisms have developed various strategies for their survival in heavy metal-polluted habitats, these organisms are known to develop and adopt different detoxifying mechanisms such as biosorption, bioaccumulation, biotransformation and biomineralization, which can be exploited for bioremediation either
ex situ or
in situ [
24,
25,
26,
27]. A global survey to examine the use of bioremediation technologies for addressing the environmental problems was carried out by Elekwachi
et al. [
28]. They found that despite aspirations from respondents to apply bioremediation techniques, it should not become the current practice. Developed economies made higher use of low-cost
in situ bioremediation technologies such as monitored natural attenuation, while their developing counterparts appeared to focus on occasionally more expensive
ex situ technologies. Despite significant investment and widespread availability of online resources, their limited use underlines the need to explore improved training and development of more user-friendly resources. There are many reports about biodegradation and bioremediation strategies being utilized by bacteria or plant species [
29,
30,
31,
32], but so far none of these investigations suggest possible drivers in the global use of the said techniques [
28]. Among the preferred methods for treatment of contaminated areas, 51% of the respondents preferred environment friendly approaches, including microbial remediation (35%) and phytoremediation (16%) [
33,
34].
Microorganisms uptake heavy metals actively (bioaccumulation) and/or passively (adsorption) [
35]. The microbial cell walls, which mainly consist of polysaccharides, lipids and proteins, offer many functional groups that can bind heavy metal ions, and these include carboxylate, hydroxyl, amino and phosphate groups [
36]. Among various microbe-mediated methods, the biosorption process seems to be more feasible for large scale application compared to the bioaccumulation process, because microbes will require addition of nutrients for their active uptake of heavy metals, which increases the biological oxygen demand or chemical oxygen demand in the waste. Further, it is very difficult to maintain a healthy population of microorganisms due to heavy metal toxicity and other environmental factors [
37,
38]. Fungi of the genera
Penicillium,
Aspergillus and
Rhizopus have been studied extensively as potential microbial agents for the removal of heavy metals from aqueous solutions [
39,
40]. Xiao
et al. reported a novel technology for obtaining highly efficient biosorbents from endophytes, a hyperaccumulator, which is more convenient than the traditional method of obtaining biosorbents [
41]. Sun
et al. evaluated the genetic diversity of endophytic bacteria from the copper-tolerant species of
Elshotzia apliendens and
Commelina communis, reporting increased dry weights of roots and aboveground tissues compared to uninoculated plants [
42]. Further, they also reported significant amounts of (ranging from 63% to 125%) Cu content in inoculated plants compared to uninoculated ones.
In view of such reports on the use of microorganisms and plants for removal of heavy metals from contaminated sites, the present review focuses on recent developments in bioremediation techniques. Additionally, new approaches such as the designer plant approach and rhizosphere modification to achieve the goal of bioremediation in a cheaper and safer way are also discussed.
4. Phytoremediation
Phytoremediation basically refers to the use of plants and associated microorganisms to partially or completely remediate selected contaminants from soil, sludge, sediments, wastewater and ground water. It can be used for removal of radionuclides, organic pollutants as well as heavy metals [
92]. Phytoremediation utilizes a variety of plant processes and the physical characteristics of plants to aid in remediation of contaminated sites. Over the recent years, a special emphasis has been placed on phytoremediation since this property can be exploited for remediation of heavy metal polluted soils [
93,
94]. It is a cost-effective, efficient and eco-friendly
in situ remediation technology driven by solar energy. The technique of phytoremediation includes a number of different processes such as phytoextraction, phytofiltration, phytostabilization, phytovolatilization and phytodegradation [
95]. A summary of various processes involved in the phytoremediation of heavy metals is shown in
Figure 2. The initial step of phytoremediation is phytoextraction, the uptake of contaminants from soil or water by plant roots and their translocation to and accumulation in biomass,
i.e., shoots [
96]. Translocation of metals to shoots is an important biochemical process and is desirable in an effective phytoextraction. The next important process of phytoremediation is phytofiltration, which includes rhizofiltration (use of plant roots), blastofiltration (use of seedlings) or caulofiltration (use of excised plant shoots) [
97]. In this, the metals are absorbed or adsorbed and thus their movement in underground water is minimized. In addition to the above process, phytostabilization or phytoimmobilization occurs, which reduces the mobility and bioavailability of metals in the environment and thus prevents their migration into groundwater or the food chain [
98]. Plants perform the immobilization of heavy metals in soils by sorption through roots, precipitation, complex formation or metal valence reduction in the rhizosphere [
99]. Organic pollutants taken by plants are metabolized by enzymes such as dehalogenase and oxygenase, which are not dependent on rhizospheric microorganisms [
100]. However, several heavy metals absorbed by plants get converted into volatile forms and subsequently released into the atmosphere by the process called phytovolatilization. This process has been used for removal of some volatile heavy metals like Hg and Se from polluted soils [
101]. However, this is limited by the fact that it does not remove the metals completely but rather transfers them from one medium (soil or water) to another (atmosphere) from which they can reenter soil and water.
Recently, removal of heavy metals through phytoremediation, especially hyperaccumulators to degrade and detoxify contaminants, has received wide attention due to its efficacy and cost efficiency [
51]. The criteria used for hyperaccumulation varies according the metal, ranging from 100 mg·kg
−1 dry mass for Cd to 1000 mg·kg
−1 for Cu, Co, Cr and Pb. These values exhibit a shoot-to-soil ratio of metal concentration and the factor for bioaccumulation is higher than 1 [
102].
Figure 2.
Various processes involved in the phytoremediation of heavy metals.
Figure 2.
Various processes involved in the phytoremediation of heavy metals.
Hyperaccumulators have been found to exhibit higher heavy metal tolerance and accumulating abilities compared to other plants [
103]. Many such plants like
Arabidopsis halleri [
104] and
Solanum nigrum L. [
105] have been utilized for phytoremediation of cadmium.
Table 2 summarizes the list of different plants reported for remediation of heavy metals. However, the disadvantages that limit the use of hyperaccumulators include difficulty in finding heavy metal hyperaccumulators, slow growth and lower biomass yield. This makes the process quite time-consuming and therefore not feasible for rapidly contaminated sites or sewage treatments [
41]. However, different rhizospheric microorganisms that may play important roles in plant growth and/or metal tolerance via different mechanisms are known, and these can be beneficial for the design of a phytoremediation plan to select appropriate multifunctional microbial combinations from the rhizosphere, which may include arbuscular mycorrhizal fungi and plant growth-promoting rhizobacteria. It is suggested that the remediation role of rhizosphere is the main part of phytoremediation and one of the main basic theories for removing contaminants by the combined activity of plants and microorganisms [
106]. The main reason for the enhanced removal of metals in the rhizosphere is likely the increase in the number and metabolic activities of microorganisms. In the rhizospheric degradation process, the metal toxicity to plants can be reduced by the use of plant growth-promoting bacteria, free-living soil microorganisms that exert beneficial effects on plant growth. In this process, plants can stimulate microbial activity about 10–100 times by the secretion of exudates which contain carbohydrates, amino acids, flavonoids
etc. [
107]. In return, the rhizosphere bacteria that contain ACC deaminase may act to insure that the ethylene level does not impair root development and to facilitate the generation of larger roots which enhance seedling survival [
108]. It is reported that nickel-resistant soil bacterium
Kluyvera ascorbata SUD 165 promoted the growth of
Brassica campestris in the presence of high concentration of nickel due to its ability to lower the level of ethylene stress in the seedlings [
109].
Table 2.
List of selected plants reported for phytoremediation of heavy metals.
Table 2.
List of selected plants reported for phytoremediation of heavy metals.
Heavy Metal | Plant Species | Ref. |
---|
Cd, Cu, Pb, Zn | Salix spp. (Salix viminalis, Salix fragilis) | [110,111,112] |
Cd | Castor (Ricinus communis) | [113] |
Cd, Pb, Zn | Corn (Zea mays) | [114] |
Cd, Cu, Pb, Zn | Populus spp. (Populus deltoides, Populus nigra, Populus trichocarpa) | [112] |
Cd, Cu, Ni, Pb | Jatropha (Jatropha curcas L.) | [115,116] |
Hg | Populus deltoides | [117] |
Se | Brassica juncea, Astragalus bisulcatus | [118] |
Zn | Populus canescens | [119] |