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Review

Bioremediation of Aquatic Environments Contaminated with Heavy Metals: A Review of Mechanisms, Solutions and Perspectives

by
Carolina Faccio Demarco
1,
Maurízio Silveira Quadro
2,
Filipe Selau Carlos
3,
Simone Pieniz
4,
Luiza Beatriz Gamboa Araújo Morselli
1 and
Robson Andreazza
1,*
1
Technology Development Center, Graduate Program of Science and Materials Engineering, Brazil Federal University of Pelotas, Pelotas 96015-560, Rio Grande do Sul, Brazil
2
Engineering Center, Federal University of Pelotas, Pelotas 96015-560, Rio Grande do Sul, Brazil
3
Faculty of Agronomy, Federal University of Pelotas, Pelotas 96015-560, Rio Grande do Sul, Brazil
4
Faculty of Nutrition, Federal University of Pelotas, Pelotas 96015-560, Rio Grande do Sul, Brazil
*
Author to whom correspondence should be addressed.
Sustainability 2023, 15(2), 1411; https://doi.org/10.3390/su15021411
Submission received: 22 November 2022 / Revised: 30 December 2022 / Accepted: 5 January 2023 / Published: 11 January 2023
(This article belongs to the Special Issue Heavy Metal Contamination and Phytoremediation of Soil and Water)
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Abstract

:
The degradation of water resources is related to anthropic actions such as rapid urbanization and industrial and agricultural activities with inefficient land use and occupation management. Water pollution caused by organic and inorganic contaminants represents a current challenge for researchers and humanity. One of the techniques used to remove pollutants from aquatic environments is bioremediation, through the metabolism of living organisms, and especially phytoremediation, with plants as a decontamination agent. Aiming to demonstrate the current mechanisms, solutions, and perspectives regarding bioremediation, and especially phytoremediation in aquatic environments, a literature review was conducted, highlighting the following subjects: heavy metals as contaminants, phytoremediation, evaluation of resistance mechanisms, removal of heavy metals by microorganisms and biofilters of the artificial floating islands type. From the literature research carried out, it can be concluded that alternatives such as macrophyte plants have proved to be an effective and efficient alternative with a high potential for removal of contaminants in aquatic environments, including concomitantly with microorganisms. There was no mechanism well-defined for specific absorption of heavy metals by plants; however, some results can indicate that if there was sporadic contamination with some contaminants, the plants can be indicators with some adsorption and absorption, even with low concentration in the watercourse by the moment of the evaluation. It is necessary to study bioremediation methods, resistance mechanisms, tolerance, and removal efficiencies for each biological agent chosen. Within the bioremediation processes of aquatic environments, the use of macrophyte plants with a high capacity for phytoremediation of metals, used combined with bioremediating microorganisms, such as biofilters, is an interesting perspective to remove contaminants.

1. Introduction

The degradation of water resources is intrinsically related to rapid urbanization, industrial activities, agriculture, and the formation of urban agglomerates together with inefficient management of land use and occupation [1]. The release of pollutants through vehicular emissions, inadequate disposal of solid waste, chemical industries, and mining activities, commonly affect soil and, consequently, water quality due to the addition of heavy metals (HM) and other compounds [2]. Furthermore, urban land made a disproportionately large contribution to water pollution compared to other kinds of land use because intensive anthropogenic activities and urbanization can exacerbate the negative impacts on water quality [3].
Water pollution by organic and inorganic contaminants represents a current challenge, and the attempt to remove these elements is the object of study of different studies [4]. Several pollutants have recently been analyzed in the literature for their remediation by biological agents, such as pharmaceuticals and cosmetics [5]; polycyclic aromatic hydrocarbons [6]; artificial chemicals [7]; microplastics [8]; agrochemicals and pesticides [9]; primary nutrients [10]; HM [8,11,12,13,14,15].
Bioremediation is the most common ecologically sound biological technique to improve the natural degradation process [16]. Contamination through HM in soil and water is a major problem in developing countries, so phytoremediation is the best possible method for regions with large and moderate levels of concentration, rather than regions with high concentrations in little volume [17]. HM have properties of non-biodegradability, toxicity, and bioaccumulation potential, thus representing a threat to the environmental quality and health of the population [18]. The removal of HM from the medium—both aqueous and soil, can be performed by the metabolism of living organisms. This technique is called bioremediation and can use fungi, yeasts, bacteria, algae, cyanobacteria, and plants for the removal of the contaminant [19].
Phytoremediation is one of the bioremediation techniques and consists of the application of plants as a decontamination agent, especially aquatic macrophytes, which have the potential for removal of HM and other contaminants in the environment, serving as natural filters in contaminated areas [20]. Studies demonstrate that nutrients such as phosphorus and nitrogen can be absorbed naturally [21], as well as HM [22]. Aquatic macrophytes form a complex ecosystem based on symbiotic interaction with different microorganisms, both in natural conditions and in-built wetland systems [5].
One of the forms of applicability of living plants for remediation of contaminated water bodies is floating island biofilters. The system consists of a device where the plants remain floating in the water column and the roots perform filtration and allow the formation of biofilm of microorganisms [21]. For the effective use of this system, it is necessary to remove the plants after the limited capacity of removal of contaminants, to avoid the re-entry of the compounds into the water column due to the process of decomposition of the plant tissues [23,24]. The choice of the best method for the treatment of biomass after phytoremediation is hard to make, considering that simple combustion and gasification require a lot of care, in addition to the environmental impact caused by ash and gases [17]. The proper disposal of this biomass after removal is a key part of ensuring that there is no generation of secondary pollution and, at the same time, allows the generation of value-added by-products. For a sustainable remediation system, it is important to use plants with rapid growth and greater biomass accumulation [20].
Some studies have already demonstrated the conversion of macrophyte biomass into adsorbents, biogas production, and biochars, among others [5,21,24,25]. This conversion of biomass meets the circular economy and clean production and requires further studies for effective application [25]. Aiming to demonstrate the current mechanisms, solutions, and perspectives regarding bioremediation, and especially phytoremediation in aquatic environments, a review of the scientific literature was conducted, addressing aspects such as contaminants, phytoremediation, evaluation of resistance mechanisms, removal of HM by microorganisms and biofilters of the artificial floating islands type.

2. Heavy Metals (HMs) as Contaminants

HM is a general description for metals that are relative to high densities, atomic weights, or atomic numbers; however, for environmental studies, this term is well-used for indicating toxicity for living organisms and as a hazardous substance. Many HMs are nutrients and with high concentrations are contaminants such as Cu, Co, Zn, Cr and others [26]; however, other HMs do not have any function in living organisms and are toxic even in small concentrations such as As, Hg, Cd, Pb, and others [26]. For this reason, there are many studies and legislations for each element due to its concentration and form for toxicity and place found such as soil and water, for example.
The form of HM is also important once it can promote some key characteristic of this metal such as to improve toxicity or reduce mobility as in the case of chromium, once the oxidative phase Cr (VI), it is one of the most oxidative agents and can oxidate organic matter and tissues, and it can be more toxic in the environment, and Cr (VI) has been identified as a “Group I human carcinogen” with multisystem and multiorgan toxicity [27]. On the other hand, Cr (III) has been recommended for years as a trace element necessary for the proper functioning of organisms [28]; however, high concentrations can promote problems for living organisms and the environment.
When HMs are soluble in the watercourse, the problem of the contaminants can be exponentially increased once the solubility for microorganisms, plants, fish, and humans is increased, and all the food chain can be contaminated and biomagnification can be improved. For this reason, legislation of many governments has tables of toxicity for reference of pollution such as in Brazil [29] and in the USA [30], where limits on soil and water are proposed. These limits can be variable because of the exposure and characteristics of the watercourse, use, and limits in the country and or State.
Rivers and lakes have received high amounts of toxic metals, but more studies are necessary on the adsorption and transformation of these metals in the hyporheic zone and the exchange flux between the sediment–water interface. Fine sediments and colloidal particles can act as a carrier of HM, which may lead to higher accumulations of contaminants in the hyporheic zone and in the water itself [31]. It is important to know that the same HM that is adsorbed into a colloidal system, can be a source for delivery of this contaminant to the system and come back to the intoxication of the living microorganisms.
HMs are elements naturally appearing in the environment with a release that can be from natural origin, by weathering of rocks and pedogeneses, or by anthropogenic activities, such as industrial activities and inappropriate disposal of effluents [32]. HM pollution represents a great risk due to its potential permanence in the environment and bioaccumulation in plants and animals in their trophic chains, causing damage to organisms even at low concentrations [33].
The consequences of the presence of excessive concentrations of HM in the human body are, in general: damage to the kidneys and bones, endocrine, cardiovascular and neurological problems, in addition to potentiating the development of cancer [34]. Table 1 presents the HM best known for their deleterious effects on human health, in conjunction with the reference values established by the World Health Organization [35], in addition to describing the main toxicological effects on the human organism.

3. Phytoremediation in Aquatic Environments

The phytoremediation technique is based on the potential of a variable of species of plants capable to remove, stabilize or kidnap organic or inorganic compounds. It is also one of the effective methods for reducing environmental contamination by HM [11]. Thus, different species have been studied to perform phytoremediation, highlighting the hyperaccumulator species [36].
Aquatic macrophytes have properties that allow the filtration of different contaminant substances in the medium, making them favorable for application in the removal of it. The tissues of the emerging parts of these plants are responsible for storing nutrients, such as nitrogen, which has physiological and biomolecule formation functions such as amino acids, proteins, and chlorophyll; and, phosphorus, which performs various metabolic, genetic, structural, and regulatory functions in plants [37].
Responsible for promoting an environment favorable to the multiplication of microorganisms in the rhizosphere, macrophytes facilitate the retention and/or transformation of contaminants. Another characteristic is the reduction of the speed of water flow, allowing the reduction of dissolved solids and consequently reducing turbidity [38].
During bioaccumulation, macrophytes store the polluting elements in their roots or transmit them to the shoots [14]. The tissue of the submerged parts allows the expansion of the surface area for the development of microbial community biofilm and promotes the release of oxygen, increasing degradation, in addition to nutrient absorption [39]. On the other hand, the roots help in reducing the flow, allowing the sedimentation of particles in larger suspension—reducing turbidity, and also promoting the biological absorption of nutrients, functioning as filters [40].
The removal of HM from the medium requires the application of plants with a tolerance to the toxicity of these elements since some of these act as micronutrients in low concentrations, being toxic at high values; and, others do not present known biological function in plant metabolism, and may induce toxic effects even at low concentrations [41]. Therefore, considering that the response of metal accumulation mechanisms differs between species [12], plant selection should mutually consider tolerance and removal capacity for phytoremediation success [7].
Phytoremediation has the advantage of being able to be applied on-site, consequently minimizing the exposure of the contaminant to other receptors and areas, as well as its benefits to efficiency and sustainability [42]. The main phytoremediation mechanisms include phytoextraction, phytostabilization, rhizofiltration, phytovolatilization, and phytodegradation. Phytoextraction can be characterized by the removal of HM through the roots and this content is translocated to the aerial part of the plant [37]. Phytostabilization, however, is based on the use of plants aiming at conversion into less bioavailable and less mobile forms [43].
Rhizofiltration consists of filtering contaminants through the root zone. In the case of HM, there may be absorption into the roots, or adsorption on the surface of the roots. Some aspects that directly influence this mechanism are the presence of root exudates, and pH, which allow the precipitation of HM [44].
Phytovolatilization is a mechanism based on the conversion of compounds to volatile forms, which are eliminated by plants through the transpiration process. Some metals that have been studied as application potential in this technique are selenium, mercury, and arsenic [45]. Phytodegradation encompasses the degradation of the contaminant through metabolic pathways. The plant then absorbs the compounds of the medium and, with the support of different enzymes, degrades them into non-toxic forms. This technique is commonly used for organic compounds [46].

4. Evaluation of Resistance Mechanisms

An important effect caused by the presence of HM in plants is oxidative stress. This effect increases the reactive oxygen species (ROS), such as superoxide radical (O2-), hydroxyl radical (OH), hydroperoxyl radical (HO2-), peroxides (O2-2), hydrogen peroxide (H2O2), and oxygen (O2), which are responsible for causing damage such as metabolic dysfunction and even cell death [47].
It is noteworthy that ROS are part of the natural metabolism of the plant; however, the imbalance between the amount of ROS produced and the amount eliminated by enzymatic and non-enzymatic processes is the cause of oxidative stress and its respective deleterious effects [48].
The effort against oxidative stress from the antioxidant system has a direct relationship with the plant species, stage of development, and growth conditions [49]. Towards that, plant cells produce antioxidant enzymes, such as superoxide dismutase (SOD), which constitute the first line of defense against ROS, resulting in the formation of H2O2 [50]. Subsequently, there is a coordinated action of a set of enzymes including catalase (CAT), peroxidase (POD), and ascorbate peroxidase (APX) [51].
Lipid peroxidation refers to the oxidative degradation of lipids which is caused by the excessive ROS increase, damaging the structure and functioning of membranes due to changes in fluidity and permeability [52]. Malondialdehyde is among the most widely used biomarkers because it is one of the most well-known secondary products of lipid peroxidation [53]. Thus, lipid peroxidation can be estimated by measuring the formation of thiobarbituric acid reactive substances (TBARS) and quantified as malondialdehyde.
The quantification of proline contents also assists in understanding the mechanisms of resistance to HM. High levels are associated with stress resistance, since there is evidence of the increased quantity of this amino acid in plant tissues in situations of high levels of HM [51,54].
The pigments present in plants, such as chlorophyll a and chlorophyll b, are responsible for photosynthesis and are significantly affected by abiotic stresses. HM can cause inhibition of chlorophyll biosynthesis by hindering the transport chain of photosynthetic electrons, and thus the contents of these pigments in plants are inversely proportional to the concentrations of HM [55].
Phenolic compounds (PCT) have morphological and physiological importance for plants, besides serving as protection against stress from antioxidant action. These compounds are secondary metabolites and tend to break HM [56]. Manquián-Cerda et al. [57] studied the effects of heavy metal Cd on the growth of Vaccinium Corymbosum L. and verified the increase in phenolic compound contents being mediated by increased ROS.
Antioxidant activity can be evaluated by the DPPH method (2,2-diphenyl-1-picryl-hydrazyl), seen by wide application as an empirical free radical for this type of assay. The increase in DPPH elimination activity may be related to the increase in some secondary metabolites, which help in increasing antioxidant defense [58].
The resistance mechanisms can also be evaluated by anatomical characterization, a tool that allows identifying the histological changes responsible for the tolerance to HM. The most frequent changes are the accumulation of metals in specialized cells of the epidermis, trichomes, and inside the vacuole, as well as the thickening of the cell wall [59,60].
Table 2 presents several resistance mechanisms studied in aquatic macrophytes and HM.

5. Removal of HM by Microorganisms

Microorganisms have metabolic pathways that use contaminants as an energy source for their growth and development, through respiration and fermentation. However, they can also carry out degradation of the compounds through co-metabolism (without nutritional utilization of the substrate) [67].
For the efficient use of microorganisms in the removal of HM, it is necessary to make the selection of organisms resistant to the compound of interest, from the isolation technique, as well as identification of resistance mechanisms [68]. This selection can be performed in contaminated areas, which perform a natural pre-selection since they are more likely to have organisms tolerant to the stress situation.
Among the strategies for the removal of HM by microorganisms, biosorption stands out, a process where (i) dead biomass, (ii) live cultures, or (iii) extracellular polymeric substances (EPS) can be used. EPS are produced by microorganisms and present in their composition mainly polysaccharides and proteins. EPS have plenty of negative charges, allowing binding with HM; therefore, they have the potential for removal of these ions from aqueous solutions [69]. The EPS matrix confers mechanical resistance, and water and nutrient retention, and assists in the resistance of cells to various stress conditions [23].
It is noteworthy that, for biosorption to be efficient, it is necessary to analyze the physical nature of biosorbents, sorption kinetics, maximum adsorption capacity, as well as the regeneration capacity of the adsorbent and the stability of microorganisms as biosorbents [70]. Among the bacteria commonly used for metal biosorption are the genera Bacillus, Pseudomonas, and Streptomyces [71].
Some mechanisms of resistance of living microorganisms to heavy metal ions are illustrated in Figure 1. Active export of metal ions depends directly on special resistance genes on the chromosome or plasmid. These genes encode heavy metal transporters, performing the ion influx. For instance, one can cite enzymes called P-type ATPase, which transport specific ions through the cell membrane against a concentration gradient [72].
Extracellular sequestration of ions is responsible for reducing the toxicity of these elements to microorganisms. This mechanism allows the accumulation of HM in different biological structures and can be performed, for example, by EPS, glutathione, and biosurfactants [73].
The sequestration of metal ions can also be performed intracellularly, when the element is already inside the cell, preventing more sensitive cellular components from being affected by toxicity. In this mechanism, ions can be accumulated by cysteine-rich proteins such as metallothioneins (MTs), which have a high affinity for free metal ions [74].
Enzymatic detoxification regulates the chemical transformation of HM into less toxic forms, conferring the ability to tolerate HM by microorganisms [75]. The mechanism is based on the redox state change, where enzymes perform oxidation and reduction reactions of metal ions. An example is the bacterium Bacillus sp., which is resistant to mercury by Hg reductase, responsible for reducing mercury to the metallic state, released into the medium through the cell membrane [73]. The presence of cationic diffusion facilitating transporters (CDF) is also involved in resistance to HM by the flow of ions [76].
The joint use of aquatic macrophytes and microorganisms—such as bacteria originating from the rhizosphere—represents a solution for the removal of HM in contaminated water bodies. Or, in the removal of polycyclic aromatic hydrocarbons (PAH), as was the case with the study by Yan et al. [6], with the use of macrophytes Vallisneria natans and Herbaspirillum bacteria, which made use of PAH as a carbon source and promoted plant growth. Recent studies demonstrate that bacterial inoculation enhances the natural remediation ability that aquatic plant species have, making them more resistant and increasing the ability to remove these compounds [77]. Rhizopheric microorganisms, such as denitrifying bacteria, can affect “rhizobio growth” in aquatic plants, boosting wastewater purification, such as the study by Lu et al. [78], with the use of the inoculated Pseudomonas rhizospheric strain and Spirodela polyrrhiza in nitrogen removal. Therefore, the interaction between macrophytes and microorganisms can help create new environmental decontamination strategies [6].

6. Artificial Biofilter Floating Islands

Biofilter floating island systems are a variation of the wetland system built to improve water quality. They are made of vegetation on floating support, remaining under the surface of the water body [79] (Figure 2).
These AFI systems showed the upper part of the vegetation growing above the water level, while the roots perform the filtration of contaminants in hydroponics. The roots allow the development of a biofilm of microorganisms, which also present mechanisms for the removal of contaminants [80,81]. The types of support that can be used are usually fabricated of materials such as polymers, wood, and fiberglass, and present fluctuation by foam injection or use of hollow and sealed components [40]. Different species of aquatic macrophytes have been used for the remediation of water bodies, such as water hyacinth (Eichhornia crassipes), lentil (Lemna, Lemna spp.), water lettuce (Pistia stratiotes), vetiver grass (Chrysopogon zizanioides) and reed (Phragmites australis) [82] and could be applied in artificial islands biofilters.
The use of combined technologies, such as the addition of biofilms or immobilized microorganisms, can increase the potential for removing contaminants from floating islands [83]. In the literature, the use of immobilized denitrifying bacteria, the inclusion of an aeration system, addition of rice straw and other fibers as substrates have been reported, aiming to improve the functioning of these filter systems [84].
After the process of removing contaminants, biomass must be removed from the water body before the decay phase occurs and the nutrients and HM removed reenter the system [85]. Regarding the part of the plant to be removed, some studies have already shown that, during the initial phase of plant growth, the highest concentrations of nutrients are in the aerial part, while in the senescence phase, there are higher concentrations in the roots [86]. Thus, the need for further studies is highlighted, given the capacity of contaminant retention in both parts of the vegetable [23].
It is important to know about floating islands, including their place of study, composition material, species used, and parameters analyzed, as presented in Table 3.
The disposal of biomass after the removal of contaminants will depend on the characteristics and toxicity of the material since there is a possibility of secondary contamination. The possibilities of application/disposal of this biomass range from anaerobic fermentation, composting, combustion, phytomining, landfill, and pyrolysis [95]. Among them, pyrolysis stands out for being suitable for biomass containing HM, given the ability to promote the stabilization of metals within the carbon matrix, according to a study performed by Huang et al. [96]. Pyrolysis of biomass is responsible for reducing the mass of residues and degrading the material in pyrolytic products of added value, giving rise to the so-called biocoal, which can be used as corrective for the soil, considering the presence of basic nutrients with N, P, and K, among others [97].

7. Advantages and Disadvantages of Bioremediation

Bioremediation using only plants or its combination with microorganisms such as fungus or bacteria has an important advantage against the conventional remediation treatment, once the society is more suitable and can choose biological treatments against the conventional. The bioremediation issue for studies and applications has increased in the current years. Studies with the most different applications such as heavy metals [98,99], hydrocarbonates [100], diesel [101,102], biodiesel [101,102], persistent organic pollutants [103], pesticides [104], and others.
Phytoremediation is one of the main techniques of bioremediation applied for the removal of contaminants from the environment, once to apply bacteria, fungus and other microorganisms have some limitations for applications in the environment. The use of macrophytes as a cost-effective bioremediation method is an interesting technique to treat contaminated water [20]. According to Shen et al. [105], biological, physical, chemical, agronomic, and genetic approaches have been used to enhance phytoremediation. Nevertheless, bioremediation systems require plants with rapid growth and higher biomass accumulation [20].
It is important to understand the limitations of each technique once the microorganisms contaminate other environments, or cause other problems, e.g., the application of one bacterium such as Pseudomonas pneumoniae in the environment for removal of copper [106], and to know that this kind of bacteria can promote diseases in humans.
Another disadvantage is the disposal methods of contaminated biomass, such as pyrolysis, incineration, composting, and compaction, which can be effective. However, they are costly and can provide security issues with improper disposal of contaminated HM [105]. Although the biomass of these wetland plants may be used for bioenergy generation [15], it is paramount to develop research for new and economical technologies to convert the contaminated waste from bioremediation to benefit the environment.
Plants that can be seen in their growth, and measured the population, are more suitable to understand for controlling some undesirable growth or population and to reintroduce the plants for phytoremediation. Phytoremediation has the potential to remove high concentrations of contaminants from soil; despite this possibility, long-term treatment is necessary once with the time course to decrease the concentration and efficiency. Meanwhile, in the watercourses, the possibility to introduce and remove plants is more suitable for remediation and can be easily used and managed, and it can increase the results and reduce the time course of the bioremediation process. This kind of study should be well explored and used in the field.

8. Conclusions and Future Prospects

The increase in environmental contamination has culminated in a reduction in the quality of soils and aquatic environments throughout the globe. Alternatives such as macrophyte plants have been used for phytoremediation of these environments, and are an effective, efficient alternative with high potential for use. Not all plants can absorb and or adsorb toxic HM from the environment; however, by studying bioremediation methods for these metals, it is possible to highlight various resistance mechanisms and forms of bioremediation that are fundamental to the identification of the best use of the plant. Allied to plants, resistant microorganisms can exert various forms of bioremediation, helping the plant extract, modify or mitigate the toxic effect of HM. Once this step has been identified, phytoremediation can be improved by transporting or reducing the toxicity of HM.
The relationship between the type of contaminant with the phytoremediation plant affects the capacity and mechanism of bioremediation. In addition, with different contaminants, this dynamic is also affected. This theme still needs many studies to reach a common denominator, even if there would have more results, they would hardly find an exact formula because they are living organisms in often complex environmental interactions, such as type of organism, different temperatures (including on the same day), different floating concentrations of HM, and different volumes and pHs, among other environmental variants. To reduce these processes, it is recommended that, when using plants and microorganisms, they are adapted to the environment and contamination conditions.
Within the bioremediation processes of aquatic environments, the use of macrophyte plants with a high capacity for phytoremediation of metals, used with bioremediating microorganisms, such as biofilters, is an interesting perspective to remove contaminants in solution. It is still possible to promote the use of biofilters with the incorporation of renewable materials, such as polyurethane foams, which act as adsorbents in aquatic environments. Thus, the set of environmental technologies favors remediation and bioremediation of contaminated environments.

Author Contributions

Conceptualization, C.F.D. and R.A.; methodology, C.F.D.; investigation, C.F.D., M.S.Q., F.S.C., S.P., L.B.G.A.M. and R.A.; resources, R.A.; writing—original draft preparation, C.F.D.; writing—review and editing, C.F.D., F.S.C., L.B.G.A.M. and R.A.; supervision, R.A. All authors have read and agreed to the published version of the manuscript.

Funding

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance code 001, by the CNPq (National Council for Scientific and Technological Development) and FAPERGS (Research Support Foundation of the State of Rio Grande do Sul).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Mechanisms of detoxification of metal ions by microorganisms, where (A) active heavy metal ion, (B) active export, (C) heavy metal sequestration (D) control uptake (E) enzymatic detoxification, and (F) extracellular polymeric substances—EPS.
Figure 1. Mechanisms of detoxification of metal ions by microorganisms, where (A) active heavy metal ion, (B) active export, (C) heavy metal sequestration (D) control uptake (E) enzymatic detoxification, and (F) extracellular polymeric substances—EPS.
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Figure 2. Representation of an artificial floating island (AFI), presenting (A) shoots, (B) floating device, (C) roots under the surface water, allowing biofilm formation. The system remain floating in water flow (D).
Figure 2. Representation of an artificial floating island (AFI), presenting (A) shoots, (B) floating device, (C) roots under the surface water, allowing biofilm formation. The system remain floating in water flow (D).
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Table
Table 1. Reference values in drinking water and toxicological effects of some HM on human health.
Table 1. Reference values in drinking water and toxicological effects of some HM on human health.
ElementReference Value (mg L−1)Toxicological Effects
As0.01Changes in skin pigmentation; lesions on the palms of the hands and feet; effects on the renal, gastrointestinal and cardiovascular system, as well as increased blood pressure; carcinogenic. Pregnant women with exposure to As have an increased risk of abortion or premature birth.
Cd0.003Renal dysfunction with impaired resorption of proteins, glucose, and amino acids; pulmonary alterations; carcinogenic.
Cr0.05Respiratory, intestinal, gastrointestinal, and cardiovascular problems; skin irritation; carcinogenic.
Cu2.0Gastrointestinal bleeding; hepatocellular toxicity; acute renal failure; anemia; breathing problems.
Pb0.01Brain damage to the fetus; affects the kidneys and circulatory and nervous systems.
Hg0.006Toxic effects on the nervous, digestive, and immune systems and lungs, kidneys, skin, and eyes.
Source: adapted from WHO [35].
Table
Table 2. HM tolerance mechanisms in aquatic macrophytes.
Table 2. HM tolerance mechanisms in aquatic macrophytes.
SpeciesMetalConcentrationToxicological EffectsReference
Macleaya cordataMn2+0–12 mmol L−1Cells distort and deform, black precipitates appeared in the intercellular space, mitochondria, and starch granules decrease.
Chloroplasts shrink, and hungry particles increase.		[61]
Nerium indicumPb
Zn
Cu
Cd		3311.5–4297.08 mg kg−1
1398.33–1704.92 mg kg−1
143.33–163.5 mg kg−1
28.92–43.83 mg kg−1		Significant decrease in the acid-extractable state, a significant increase in the residue state, and a small decrease in the Fe-Mn binding state, and a small increase in the organic binding state.[62]
Pontederia cordataCd2+0–66 mMDecrease in chlorophyll contents due to increased lipid peroxidation and inhibition of biosynthesis of chlorophyll precursors; inhibition of Cd translocation from roots to aerial part; SOD and POD activities without variation about control at concentrations 0.04 mM to 0.22 mM in 15 days of exposure;A concentration of 0.44 mM caused a reduction in SOD and POD.[63]
Potamogeton
pectinatus L.		Cu0–1000 μMAccumulation mainly in the roots; dose-dependence pattern identified; decreased levels of chlorophylls and carotenoids; Inhibition of photosynthesis; leaf damage; reduction in pigments.[64]
Nymphaea tetragonaU0–55 mg L−1Increased activity POD, CAT, SOD; increased MDA levels aggravate cell membrane damage; inhibition of soluble protein, chlorophyll a, chlorophyll b, and carotenoid sums.[65]
Spirodela polyrhiza L. Cu2+ Hg2+0.0–40 μM
0.0–0.4 μM		Increased SOD activity in 10 μM Cu+2; 0.2 μM Hg+2; CAT, at 20 μM Cu+2; 0.2 μM Hg+2 and GPOD, at 10 μM Cu+2; 0.2 μM Hg+2 with the fall of all activities until 40 μM Cu+2 and 0.4 μM Hg+2.[66]
Source: The authors.
Table
Table 3. Studies carried out with artificial floating islands.
Table 3. Studies carried out with artificial floating islands.
Study AreaScaleFloating MaterialPlant SpeciesPlanting MethodEvaluated ParametersRef.
Botanical Garden (Pakistan)MicrocosmContainer/plastic tub of 50 L capacitySalvinia natans; Pistia stratiotesAdult plantsP-accumulated in plant biomass; pH; temperature.[87]
River (South Africa)In situFree-floating macrophytesPontederia (=Eichhornia) crassipes; Stuckenia pectinatus; Typha capensis; Cyperus sexangularis;
Phragmites australis		Adult plantspH; chemical oxygen demand (COD), Zn; Fe; Cd; As; Cr; Pb; Hg; Cu.[1]
Botanical Garden (China)In situContainer, ecological floating bedVallisneria natans; Ludwigia adscendens; Ipomoea aquatica;
Monochoria vaginalis; Saururus chinensis; Acorus calamus;
Typha orientalis;
Schoenoplectus juncoides		Adult plantsTotal nitrogen (TN), total phosphorus (TP), COD.[88]
Rural area (China)In situPVC tubes (40 mm) and ropesOenanthe javanica; Gypsophila sp.; Rohdea Japônica; Dracaena sanderiana; Gardenia jasminoides Var. grandiflora; Gardenia jasminoides
Var. prostratae Salix Babylonica.		SeedlingsTemperature, pH, OD, SS, COD, N total; P total; chlorophyll a.[89]
Aquaculture effluent channel (Italy)In situLicence Tech-IA® (EVA)Phragmites australis; Carexelata; Juncus effusus; Typha Latifolia; Chrysopogon zizanioides;
Sparganiumerectume Dactylisglomerata		Adult plantspH, temperature, conductivity, DO, BOD, COD, N total, KTN, N ammoniacal, nitrate, P total, SS.[90]
Synthetic rainwater experiment (New Zealand)Mesocosma license BioHaven®Carexvirgata; Cyperus Ustulatus; Juncusedgariae; Schoenoplectus Tabernaemontani.SeedlingsCu, Zn, turbidity, temperature, DO, pH, macronutrients, and micronutrients.[91]
Nutrient Solution Experiment (China)Microcosma license BioHaven®Cannageneralis; Scirpusvalidus; Alternanthera Philoxeroides;
Cyperus Alternifolius;
Thalia Geniculata.		Adult plantsBOD; COD; N total; P total; ammoniacal N and nitrate.[92]
Urban stormwater runoffMesocosmExtruded Polystyrene Circular BuoyJuncus Effusus Carex Riparia.Pozzolan as substrate with seedlingsCd, Ni, Zn, biomass production.[93]
Urban retention ponds (USA)MesocosmCoconut fiber bristles RoLankaTM Inc.Pontederia cordata L., Schoenoplectus tabernaemontaniSeedlingsP total, P particulate, orthophosphate, N total, organic N, ammoniacal N, nitrate, chlorophyll a.[94]
Legend: Ref: reference; DO: dissolved oxygen (mg L−1); BOD: biochemical oxygen demand (mg L−1); COD: chemical oxygen demand (mg L−1); SS: suspended solids; KTN: Kjeldahl total nitrogen; a Interlaced polyester fiber (95% porosity) injected with polystyrene foam to provide buoyancy. Source: Adapted from Pavlineri, Skoulikidis, and Tsihrintzis [94].
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Demarco, C.F.; Quadro, M.S.; Selau Carlos, F.; Pieniz, S.; Morselli, L.B.G.A.; Andreazza, R. Bioremediation of Aquatic Environments Contaminated with Heavy Metals: A Review of Mechanisms, Solutions and Perspectives. Sustainability 2023, 15, 1411. https://doi.org/10.3390/su15021411

AMA Style

Demarco CF, Quadro MS, Selau Carlos F, Pieniz S, Morselli LBGA, Andreazza R. Bioremediation of Aquatic Environments Contaminated with Heavy Metals: A Review of Mechanisms, Solutions and Perspectives. Sustainability. 2023; 15(2):1411. https://doi.org/10.3390/su15021411

Chicago/Turabian Style

Demarco, Carolina Faccio, Maurízio Silveira Quadro, Filipe Selau Carlos, Simone Pieniz, Luiza Beatriz Gamboa Araújo Morselli, and Robson Andreazza. 2023. "Bioremediation of Aquatic Environments Contaminated with Heavy Metals: A Review of Mechanisms, Solutions and Perspectives" Sustainability 15, no. 2: 1411. https://doi.org/10.3390/su15021411

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