Toxicity of Silver Nanoparticles and Their Removal Applying Phytoremediation System to Water Environment: An Overview

Journal of Environmental Treatment Techniques

2020, Volume 8, Issue 3, Pages: 978-984

J. Environ. Treat. Tech.

ISSN: 2309-1185

Journal web link: http://www.jett.dormaj.com

Toxicity of Silver Nanoparticles and Their Removal

Applying Phytoremediation System to Water

Environment: An Overview

1,2

Zainab Mat Lazim , Salmiati *, Abdul Rahman Samaluddin , Mohd

Razman Salim , Nor Zaiha Arman

Department of Water and Environmental Engineering, School of Civil Engineering, Faculty of Engineering, Universiti Teknologi Malaysia, Johor Bahru,

Malaysia

Institute Centre for Environmental Sustainability and Water Security (IPASA), Universiti Teknologi Malaysia, Johor Bahru, Malaysia

Civil Engineering Department, Faculty of Engineering, Technology and Built Environment, UCSI University, Cheras, Kuala Lumpur, Malaysia

Received: 13/02/2020

Accepted: 17/06/2020

Published: 20/09/2020

Abstract

The widespread use of silver nanomaterials potentially harms the health of the whole ecosystem, especially the aquatic environment.

Silver nanoparticles (AgNPs) are directly released into environment from washing machines, colloidal silver medicines, and other AgNPs-

containing products. Review of ecotoxicological studies and the prediction of the future environmental concentrations (PEC) shows the

presence of a toxic level of AgNPs in the surface water and reveals their effect and risks to aquatic organisms. However, the AgNPs transport

behavior, their transformation in the natural environment, and how this behavior poses a risk to human and ecosystem health are significant

issues that have not been clearly known; thus, there is a pressing need to investigate them and provide effective solutions. This study reviews

the potential of macrophytes to remove AgNPs in aqueous solutions. It also discusses the impact of AgNPs on water environments, their

toxicity to aquatic organisms, and the phytoremediation functions.

Keywords: Silver nanoparticle; Macrophyte; Phytoremediation; Surface water

bacteria, plants, fishes, etc. and, thereby indirectly to humans [13,

Introduction¹

4, 15, 16]. Thus, there is a crucial need for further research

In recent years, manufactured nanoparticles (NPs) and

aiming at understanding the environmental behavior of NPs and

predicting their environmental implications [4, 10].

nanotechnology have grown very quickly and have been broadly

used. Annually, around 500 tons of silver nanoparticles (AgNPs)

are produced, representing a major class of engineered NPs

frequently used in manufactured products and also a significant

potential for environmental impact [1, 2, 3, 4, 5, 6]. AgNPs have

widely used in different industries, medical imaging, textile,

house products, etc. because of not only their high antibacterial

properties, but also high electrical and thermal conductivity [2, 5,

The AgNPs-contaminated aquatic system is a possible route

for human exposure when it is used as a source of potable water.

Different people show different reactions to this exposure such as

rash, inflammation, swelling, and mild allergic reaction, and in

some cases, no effect is observed. Living organisms (e.g.,

microbes involving in nutrient cycle, waste composting, and other

beneficial and harmful bacteria) in the aquatic environment can

be also affected directly. Previously-conducted studies on

toxicology have proved that AgNPs can cause DNA damage,

chromosomal aberrations, and even a slight effect on the brain as

revealed by tests on rats, and also their effect on the early

development of zebrafish embryos has been confirmed. In

addition, there are some biological concerns due to the fact that

harmful microbes might become resistant toward AgNPs that are

used as anti-microbe agents and also for coating some medical

equipment.

, 8, 9, 10].

However, these AgNPs containing products mostly end up in

the environment and aquatic systems due to accidentally leakage

during the manufacturing, production, distribution and disorderly

disposal. These concerns have led to several studies investigating

the detection of the particles in the aquatic environment, the fate

and transformation of AgNPs in the aquatic environment, and the

potential environmental toxicology of these AgNPs to aquatic

organisms [11, 12]. Literature shows the extensive use of AgNPs

has exerted adverse effects on the aquatic ecosystem, especially

Corresponding author: Salmiati, (a) Department of Water and Environmental Engineering, School of Civil Engineering, Faculty of

Engineering, Universiti Teknologi Malaysia, Johor Bahru, Malaysia, and (b) Institute Centre for Environmental Sustainability and Water

Security (IPASA), Universiti Teknologi Malaysia, Johor Bahru, Malaysia. Email: salmiati@utm.my.

Journal of Environmental Treatment Techniques

2020, Volume 8, Issue 3, Pages: 978-984

Toxicity of Silver Nanoparticle

In the aquatic environment, many factors that affect the fate and

transformation can be effective on the toxicity and characteristics

of AgNPs. Many parameters, including time, influence the

presence of AgNPs in water environment, which might be still in

The toxicity of AgNPs and the dynamic nature of these

particles in complex media and living systems have been

investigated for many years; however, the risk toward human

health, particularly the mammalian cells is still unclear [17, 18,

nanoparticle

shape,

suspension

surface

water,

9].

aggregate/agglomerate, dissolved, or bound with natural organic

materials or other substances that present in the aquatic system.

Dissolution also may occur when oxidation happens, which

changes Ag0 to Ag+1. This ionic state of Ag is more toxic toward

aquatic organism; however, this oxidation process is complicated

because it depends on time and water physicochemical

characteristics [2, 20, 21, 22, 23, 24]. A number of important

studies carried out into the toxicity of AgNPs are listed in Table

Table 1: The Toxicity of AgNPs

Effects of the AgNPs

Toxicity

Studies

References

Decreased hatchability

of embryos and eye

size

Fish: Japanese

medaka

[25]

Biological systems:

virus, bacteria,

fungi, Protist,

animal cell lines,

and human cancer

cell lines

Inhibitory effect on all

biological systems

tested

[26]

Phytoremediation in Aquatic Media

Phytoremediation is a natural process through which plants

Inhibited hatchability

behavioral retardation

in early-life stages;

Effects on embryos;

Neurodevelopmental

toxicity altered

are used to remove contaminants from soil, air, and water

resources. Phytoremediation has a few types: accumulation,

degradation, stabilization, rhizodegradation, rhizofiltration, and

volatilization of the contaminant in the environment [38, 39, 40].

Generally, for water or aquatic environment remediation,

macrophytes are used as phytofiltration or rhizofiltration, which

involves the removal of contaminants by adsorption/absorption

through the plant roots. Macrophytes also do the task of

phytoaccumulation through accumulating contaminants in their

biomass such as tissues of the roots, stems, or leaves. This process

can reduce pollutants in water environments such as wetlands and

estuary areas. Phytoremediation is a useful technique for

removing pollutant from the contaminated water. These

macrophytes can go through phytomining process that refers to

harvesting back the metals from water environment for recycling

purposes [41].

The macrophytes used for rhizolfiltration of AgNPs require an

extensive root system capable of tolerating the contaminated

water source and aggressively accumulating and filtrating the

contaminants. Moreover, macrophytes are better than invasive

species that quickly reproduce for self-sustaining [42, 43, 44].

The phytoremediation of contaminated water can be normally

performed with a low cost since no expensive equipment and

chemical is needed for this process. The techniques of

rhizofiltration and phytoaccumulation can improve water and soil

quality with only a negligible site disruption [38, 40]. However,

the appropriate use of macrophytes needs more experiments,

analyses, and observations since AgNPs can negatively affect the

plants itself. Once the AgNPs enter the aquatic system, the

unclear fate and transformation of AgNPs will affect the

mechanism of this phytoremediation. AgNPs can be transformed

physically and chemically by aggregation or disaggregation,

bonding with natural organic matter, or dissolution, which affect

the stability of AgNPs, the uptake and accumulation of AgNPs by

macrophytes, their bioavailability as well as their toxicology

effect toward living organisms and phytoremediator [4, 9, 10, 45,

46, 47]. The toxicity of AgNPs prevents macrophyte from

effectively remediating the contaminated water. Microorganisms

and bacteria communities that surround and are attached to

rhizosphere are supposedly very beneficial for phytoremediation

potential; however, the toxicity of AgNPs is harmful to these

microorganism communities and affect their functioning in their

[

27, 28]

Fish: Zebrafish

locomotion

Reduced ATP content

of the cell;

Inactivate enzymes

from several cellular

Human glioblastoma pathways depolarizing

cells (U251)

human lung

fibroblast cells

and mitochondrial

membrane;

Damaging lysosomes;

Increased the

[29, 30,

31, 32]

(

IMR-90)

production of reactive

oxygen species (ROS)

in a dose-dependent

manner

Cross the blood-brain

barrier and caused

long-term contextual

memory impairment

Development of

abnormalities

Mammal: Mice

[33]

Sea urchin

[4]

[5]

Affecting prokaryotes,

invertebrates, and the

fish

Ecotoxicological

−1

ng L )

(

Reduced the zucchini

biomass and

transpiration rate

Affecting population

size of certain types of

bacteria

Plant: Zucchini

seeds

[34]

[35]

Microbial profile of

caecum

Symptom of

poison with Cd:

anxiety, color vision,

increased mucus

secretion, and death

with the open

Roach (Rutilus

rutilus) and

Goldfish (Carassius

auratus)

[36]

[37]

mouth

No bactericidal

activity in

concentration of

AgNPs up to 128μg/ml

Gram-positive and

Gram-negative

bacteria

Journal of Environmental Treatment Techniques

2020, Volume 8, Issue 3, Pages: 978-984

ecosystems [46, 48].

Then, to run the experiment, plants of the same size are chosen

and washed thoroughly by tap water and distilled de-ionized

water (DDIW) to clean from any impurities. Some other

researchers just collect the similar size of plants from the river or

actual pond and then wash them with deionized water before

keeping in a nutrient solution. The experiments are normally

performed with three to five replicates. The media sample is taken

followed by a scheduled time and the visual changes of the plants

are checked to see whether there is any toxicity effect of silver on

the plants.

At the end of the experiment, all the plants are taken out of the

media and are examined. The plants are again washed thoroughly,

then are divided into roots, stem, and leaves before air dry at room

temperature or by oven dry. All the plants parts are then ground

to get fine powder for further analyses.

The Uptake of Silver Nanoparticles in Aqueous

Solution

Plants are key assets for a successful phytoremediation. The

suitable plants must be able to clean the contaminants, especially

metal nanoparticles in water sources. Several phytoremediation

studies have been done to examine the capabilities of

macrophytes in filtrating the AgNPs-contaminated water and

wastewater. Usually, a phytoremediation study is conducted in

lab to get enough data before running for the pilot scale and real

pond or river. Different plants and methods have been

investigated to imitate and understand the natural process of

phytoremediation. Mostly all the plants used in this study are

collected from actual ponds or rivers; then, they are quarantined

in artificial ponds/aquariums before being used for further

experiments. In addition, some plants are grown in a greenhouse.

Table 2: Summary of Research Conducted into AgNPs Removal

Results

Plants

Pollutants

Methodology

(Recovery/uptake/abso

rb/ removal)

Ref.

−

0.02, 0.2, and 2 mg L

Recovery of 96% , 54%

and 20% for 0.02, 0.2, 2

mgL-1 of AgNPs

AgNPs, Ag

Pistia stratiotes (water lettuce)

[52]

(

reduction of silver nitrate by

sodium borohydride)

48 hours with a light-dark cycle

of 14-10 h

respectively

Metal level in plants is

below the LOQ (2 μg

gdry plant

AgNPs

Phragmites australis (salt marsh

plant)

−

0mg L , natural at 7 days

[49]

−

1).

Uptake of Ag :

−

Mn : 0.75 mg L

Pleuston-Limnobium

P. stratiotes and S.

natans (76%) and L.

laevigatum and E.

−1

Cu : 0.37 mg L

laevigatum, Pistia stratiotes L.,

and Salvinia natans (L.) All,

Elodea canadensis Michx.,

Najas guadelupensis (Spreng.)

Magnus, Vallisneria spiralis L.,

and Riccia fluitans L.

The mixture of colloidal

solutions of metal nanoparticles

−

Zn : 0.44 mg L

Ag + Ag2O : 0.75 mg L

At 7 days for each pollutant

[50]

(Mn, Cu, Zn, Ag + Ag

canadensis (71%).

R. fluitans (65%)

V. spiralis (59%).

−

, 10, 20, 30, 50, and 100 ppm

Ag+ in MHRFW (used Silver

nitrate).

Total silver absorbed

increases by increasing

concentration of AgNPs

Egeria densa / Elodea densa

Ag+ and AgNps (reduction of

AgNO by humic acids)

[51]

(waterweed)

, 10, 20, and 30 ppm AgNps.

At 7 days

Pistia stratiotes (water lettuce)

AgNPs (natural reducing agent,

Muntingia calabura sp. Leaves)

Removal of AgNPs for

both plants were 61%

– 10 ppb for 96 hours

This study

Eichornia crassipes (water

hyacinth)

Journal of Environmental Treatment Techniques

2020, Volume 8, Issue 3, Pages: 978-984

The control plants are also subjected to the same procedure to

assess Ag initial levels in the selected plants. For determination

of the levels of Ag and the changes of total AgNps in plants and

media, samples are subjected first to microwave digestion before

being analyzed by atomic absorption spectrophotometry (AAS)

or ICPMS (depending on the given experiment), and FEG ESEM

experiment. However, the result might be different in a higher

concentration of AgNPs.

The results of the previous study showed that P. stratiotes can

reduce the concentration of AgNPs and ions in aqueous solution.

The plants also could survive under 0.02 ppm of AgNPs;

however, the increase of the AgNPs concentration to 2 ppm

caused the plant's physical shape to be degraded over time; the

leaves were wilting, discolored, and browned as the root detached

from the aerial part of the plants [49]. While, the results of a study

conducted by Leonard Bernas [51] on phytoremediation of silver

using waterweed showed that the toxicity of silver can be seen by

a deterioration in the health of plants when exposed to silver in

concentrations as low as 5 ppm. Plant health is generally

(FEI) is also used to examine the plants [45, 49, 50, 51, 52, 53,

4]. Many types of methods have been proposed in literature to

identify the plants that can be better used for phytoremediation of

AgNps and silver ion. Each method is designed in a way to

accomplish the objective defined for that specific study. Table 2

summarizes the studies carried out to remove AgNps from water.

interrupted at concentrations of 20 ppm Ag and AgNPs, as

Plants Mechanism

The results of some studies have shown that aquatic plants

revealed by the significant browning of the leaves. Higher

concentrations of silver had a more pronounced effect on the

plants for all measurements. The E. densa tests with Ag+ at 50

and 100 ppm caused the leaves to turn brown and undergo

chlorosis (insufficient chlorophyll production by leaves) and

necrosis (cell death from toxic environments and extracellular

factors).

Therefore, the presence of Ag+ or AgNPs causes an obvious

decline in plant health over the exposure period. The obtained

results of present study show that water lettuce and water hyacinth

have almost the same percentage removal rate of 61%. This

means that the plants have almost equal ability in removing

AgNPs at low concentrations. While, Olkhovych [50] showed

that the P. stratiotes and S. natans can remove all studied metal

nanoparticles from water; however, N. guadelupensis was found

more preferable for phytoremediation of AgNPs with the removal

rate of 82%.

have the capability of removing AgNPs at a rate of around 30-

00%. This proves that aquatic plants or macrophytes are useful

in green cleaning technology.

In [42, 43, 49], macrophytes of Eichornia crassipes (water

hyacinth) and Pistia stratiotes (water lettuce) were used for

phytoremediation of AgNPs in aqueous solution. The studies

were aimed to investigate the uptake of AgNPs by water hyacinth

and water lettuce in controlled conditions and evaluate the effect

of AgNPs on plants health. These macrophytes were selected and

investigated as these two plants are known to be highly capable

of tolerating metals and aggressively accumulating contaminants

and nutrients. Moreover, they have extensive root systems, are

known as invasive species of floating macrophytes, and have

already shown promising results for heavy metal water

purification purposes.

Green technology is used to utilize plants for the extraction of

All these plants can be used for phytoremediation and have

the capability to accumulate Ag of water resources. Results

obtained from the present study investigating the accumulation or

uptake of silver by water lettuce and water hyacinth are presented

in Figure 2.

certain elements depending on their properties and capabilities. In

this regard, different plants show different results. The present

study was conducted on the removal of AgNPs using water lettuce

and water hyacinth. The obtained results are shown in Figures 1

and 2.

Figure 2: The accumulation of silver nanoparticle in leaves and roots of

water hyacinth and water lettuce

Figure 1: Removal of silver nanoparticle in aqueous solution for 96 hours

and the removal rate of the silver nanoparticle

The analysis showed that the root parts of both plants play a

significant role in the accumulation of AgNPs compared to their

aerial parts. Another study [49] used salt marsh plant as

phytoremediator, and the result showed that the accumulation was

only detected in roots and rhizomes. Any Ag was not detected in

the aerial part of the plant. However, this plant can accumulate

AgNPs only in the absence of rhizosediment. Kadukova [55]

Findings showed that both the above-mentioned plants can

survive in lower concentrations (7.0-10.0 µgL ) of AgNPs. In this

condition, contaminants are retained within the plant. This low

concentration does not exert any physical effect on the plants. The

physical form of the plants remained the same until the end of the

Journal of Environmental Treatment Techniques

2020, Volume 8, Issue 3, Pages: 978-984

claimed that metal in water can enter the plants by the intracellular

Competing interests

(symplastic) and extracellular (apoplastic) pathways. However,

The authors declare that there is no conflict of interest that

would prejudice the impartiality of this scientific work.

the cell wall of plants limits the extracellular transport in the root

and lead to lower detection of Ag in the aerial part of plants. For

this experiment, only the root parts of the plant had to submerge

in the media; thus, the majority of the accumulated metal

nanoparticles are more likely to be attached and move in through

the plant roots. Therefore, these particles have low interaction

with the aerial part of the plant since the cell wall has a high cation

exchange capacity. However, silver is known to be toxic to some

plants, inhibiting enzymes and altering the permeability of the cell

membrane wall. Thus, a number of silver species are still able to

make their way into the leaves of plants. This indicates that silver

is not necessarily bound only to the root tissue of plants. The

silver species can be transported through damaged cells or these

species can utilize transport proteins to translocate from roots to

leaves [56, 57, 58].

Authors’ contribution

All authors of this study have a complete contribution for data

collection, data analyses and manuscript writing.

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M. S. Silver nanoparticles coated with natural polysaccharides as

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specific and depends on the moment of first exposure. Marine

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Conclusion

AgNPs rapidly change in particle size and surface chemistry

upon exposure to media and interaction with their chemical

environments such as salinity and pH. These exposures need to

be considered in evaluating the hazard and risks of AgNPs toward

the aquatic ecosystem since they affect the speciation of AgNPs

and their toxicity. Toxic effects can be enhanced or decreased due

to the transformations of AgNPs in the water environment by

bioaccumulation and the dissolution of AgNPs to the formation

of Ag+ ions. On the other hand, phytoremediation is a natural

method that utilizes the plant's metabolic system to remove,

reduce, degrade, assimilate, and metabolize AgNPs in water

sources and store them in the biomass of the plants. The

appropriate selection of aquatic plants can remediate AgNPs-

contaminated water. Heavy metal contamination is a growing

environmental concern; thus, successful removal using

phytoremediation approaches with duckweeds, waterweeds,

floating, and submerge macrophytes should be studied further to

provide an environmentally benign solution to the problem.

Additional studies need to be performed using macrophytes and

similar organisms to determine the most effective way for silver

species phytoremediation.

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of silver nanoparticles on natural marine biofilm bacteria.

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H.J. Transport of citrate-coated silver nanoparticles in unsaturated

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Aknowledgment

The authors would like to acknowledge the Universiti

Teknologi Malaysia and Ministry of Education of Malaysia for

providing

Grants

Q.J130000.2422.04G06

and

Q.J130000.2522.19H06. The authors also appreciate UTM

Zamalah for providing a scholarship in favor of the undertaken

project.

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Ethical issue

Authors are aware of, and comply with, best practice in

publication ethics specifically with regard to authorship

(avoidance of guest authorship), dual submission, manipulation

of figures, competing interests and compliance with policies on

research ethics. Authors adhere to publication requirements that

submitted work is original and has not been published elsewhere

in any language.

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