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Nanomaterials and Their Toxicity
to Beneficial Soil Microbiota and Fungi
Associated Plants Rhizosphere
Mayur Mukut Murlidhar Sharma, Divya Kapoor, Rahul Rohilla,
and Pankaj Sharma
Abstract Previous decades have witnessed an exponential increase in the research
and application of nanotechnology in agricultural sector. A diverse array of nanopar-
ticles (NPs) are known to find usage in agricultural sector. Their functions can
range from water storage to delivery of nutrients and fertilizers. In addition, the
inherent possession of biocidal activity by different metal and metal oxide NPs have
put forward their application to combat different bacterial and fungal pathogens.
However, despite of several gains offered by the nanotechnological-interventions
in agricultural systems, they are also known to possess inherent toxicity towards
plant growth promoting rhizobacteria (PGPR) and beneficial fungi. The continuous
exposure of NPs lead to induction of oxidative stress, production of reactive oxygen
species, disruption of cell membrane and DNA damage in the beneficial soil micro-
biota and fungi associated to plant rhizosphere. The regular application of NPs marks
their accrual in the soil systems and their concentration keeps on increasing with each
crop cycle. In addition, they also keep on accumulating in different plant tissues,
thus can be equally lethal for the consumers. Therefore, a critical assessment of their
inherent toxicological attributes and off-target effects before their field application
is strictly needed. In this chapter, we have summarized the toxicological attributes
of different NPs towards the PGPR and beneficial soil fungi.
Keywords Nanoparticle toxicity ·Nanotoxicity ·PGPR ·Cytotoxicity ·
Genotoxicity ·Rhizosphere
M. M. M. Sharma
Department of Agriculture and Life Industry, Kangwon National University, Chuncheon, Korea
D. Kapoor · P. Sha rm a (B
)
Department of Microbiology, CCS Haryana Agricultural University, Hisar, Haryana 125004, India
e-mail: sharmap@uic.edu
R. Rohilla
Department of Zoology, CCS Haryana Agricultural University, Hisar, Haryana 125004, India
© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023
A. Husen (ed.), Nanomaterials and Nanocomposites Exposures to Plants,Smart
Nanomaterials Technology, https://doi.org/10.1007/978-981-99-2419-6_18
353
354 M. M. M. Sharma et al.
1 Introduction
The past few decades have witnessed a dramatic increase in the research and industrial
applications of nano-enabled goods. NPs are often described as particles having size
in the range of 1–100 nm whereas nanomaterials possess at least one dimension below
the size of 100 nm. The increasing number of applications assigned to different NPs
is possible due to their unique attributes comprising higher reactivity owing to their
high surface area to volume ratio, increased surface potential, tunable physical and
chemical attributes, and molecular manipulation, as equated to their bulk form [1–7].
The agricultural sector is facing a lot of problems like reduced production, reduc-
tion in agricultural land, post-harvest losses, increasing attack of pathogens, reduced
fertility, increasing incidences of plant disease and pathogen attacks [8–17]. The
application of nano-enabled goods in the agricultural sector is increasing day by
day to get rid of all such challenges. The nano-technological interventions have
proved to be a boon for agricultural sector as assessed in terms of targeted delivery,
controlled release, increasing solubility and long shelf-life [18]. The application
of nano-technological tools in agriculture aids in cost reduction of fertilizers and
pesticides. The nanomaterials are known to play a key role in agriculture at diverse
stages beginning from water storage to delivery of nutrients and fertilizers manner.
Different types of metal, metal-oxide, polymeric and engineered nano materials have
been reported for their potential in sustainable agriculture [19].
Despite of several gains offered by the nano-based tools in the sustainable agri-
culture, they are also known to possess inherent toxicity towards the plant as well
as rhizospheric microbiota. The overproduction, use, and abuse of NPs followed by
their increased usage puts forward the problem of NP accumulation in the agricul-
tural sector. Despite of the mode of application ranging from irrigation to foliar spray,
soil acts as the ultimate sink for these nanomaterials. The nano-form of any metal
is known to possess unique attributes that are absent in its bulk form, therefore, it
also possess more inherent toxicity towards any form of life as compared to its bulf
form [20]. Owing to their non-specific mode of action, the NPs are equally toxic to
the beneficial microbiota as they are to pathogenic microbes. The lower forms of
life dwelling the rhizospheric zone are known to be harbored by plant systems at
the cost of photosynthates secreted in the form of root exudates. These microbial
symbionts of plants, mainly represented by bacteria and fungi, are known to support
the growth of plant systems directly by providing a lot of growth factors and indirectly
by rendering the immunity to plant systems towards any pathogenic attack [21]. The
nanomaterials finding usage in the agricultural systems is known to damage the DNA
of plant growth promoting rhizobacteria and fungi, interfere with the cell division and
permeablize their cell membranes. The disturbance in the numbers and populations
of these rhizosphere dwelling microbes may result in altered biogeochemical nutrient
cycling and of soil contaminants, reduced plant resilience, poor plamnt health and
a decrease plant productivity. The present chapter, therefore, highlights, the toxico-
logical attributes of nanomaterials towards the beneficial soil microbiota and fungi
associated with the plant rhizosphere.
Nanomaterials and Their Toxicity to Beneficial Soil Microbiota … 355
2 Nanotechnology and Nanomaterials: An Update
Nanotechnology is discipline, engineering, and technology steered at the nanoscale,
which is nearly 1–100 nm. It constitutes of technology that is engineered by
fine-tuning discrete atoms, molecules and other such minuscule materials [7, 22].
Nanotechnology has found its application all across the established science fields
such as physics, chemistry, biology, and material science since its discovery [23–
30]. The idea behind working at such a microscopic scale started with a seminal
paper entitled “There’s Plenty of Room at the Bottom” by the physicist Richard
Feynman in 1959, long before the term nanotechnology was used. He rationalized a
method in which researchers would be able to influence and regulate distinct atoms
and molecules [31]. Over a decade later, Professor Norio Taniguchi coined the term
nanotechnology during his investigations of ultraprecise machining. Significantly, it
was the year 1981 when the advancement of scanning tunneling microscope (STM)
that can discriminate structures smaller than 0.1 nm with a 0.01 nm depth resolution
marked the beginning of modern nanotechnology. With the use of this microscope
individual atoms can be repeatedly i maged and operated as desired [32, 33].
It is difficult t o even think how small is the 100 nm is. It is 100 millionths of a
millimeter or 100 billionths of a meter. To understand just how small nanotechnology
is, here are few instructive examples: A sheet of newspaper is about 100,000 nm thick,
a strand of human DNA is 2.5 nm in diameter and a human hair is almost 80,000 nm
wide [34]. The major reason of growing interest in this field can be attributed to
the superior features for example greater strength, lesser weight, improved control
of light spectrum, and more chemical reactivity than their grander-scale counterparts
[35].
Nanotechnology is a broad term for the technology generated at a nanoscale which
is generally less than 100 nm whereas nanomaterials are typically the materials
created with at least one external or internal dimensions of 100 nm or less. They
can be in any structure of particles, tubes, rods, or fibers. Since last decade, a boom
in products produced by nanotechnology or constituting nanomaterials can be seen.
[36] Recent applications comprise of healthcare products, electronics, cosmetics,
textiles, agricultural products. For instance phosphorus, zinc, potash, calcium are
used as nanomaterials to produce nanofertilizers to help reduce agriculture waste,
silver NPs are used to reduce salinity stress and heat stress of Triticum aestivum
[37, 38]. The range of NP-based interventions, comprising nano-sized pesticides,
herbicides, fungicides, fertilizers, and sensors, have been extensively studied for
plant health management and soil enhancement to satisfy the escalating demands
of growing population (Fig. 1 and Table 1). Comprehensive understanding of plant
and nanomaterial interactions unbolts innovative opportunities toward improving
crop practices such as disease resistance, crop yield, and nutrient utilization. Despite
vast research, restricted progress has been made in evaluating the nanomaterial risk
and health hazards. NP usage in the agricultural environment extensively lacks the
transparent and precise framework for risk governance and needs close scrutiny [39].
356 M. M. M. Sharma et al.
Fig. 1 A portrayal showing different types of NPs finding application in agricultural sector along
with different methods of their synthesis
3 Nanoparticle Emission into the Environment
The application of NPs is diversifying from their use in industries to everyday house-
hold products like personal care, clothing and cleaning. Thus, their production is
steadily increasing which is also reflecting in their gradually increasing amount
in the environment and posing a threat to natural ecosystem. Over the past few
years, there is growing reports focusing on sources, fate and effects of NPs. Multiple
modelling approaches are developed to confirm the concentration of NPs in the field.
Nanomaterials and Their Toxicity to Beneficial Soil Microbiota … 357
Table 1 Different nanoparticles exhibiting plant growth promotion traits
Nanoparticle Application Plant
species/microbial
species
Advantage References
TiO2 NPs, multi
walled CNTs
(MWCNTs)
3000 mg Kg−1Red clover Increased nitrogen
fixation and no
toxic effect on plant
biomass
[40]
ZnO quantum dot
nanoparticles
(QD NPs)
10.66
5.75 μg/ml
Microsporum
gypseum,
Microsporum canis,
Trichophyton
mentagrophytes,
Candida albicans,
and Candida
tropicalis
Antifungal
activities
[41]
SiO2 NPs 0.10 and 0.20
gl− 1 Fusarium
oxysporum f.
sp. lycopersici (Fo l )
and Alternaria
solani (As)
Increased plant
growth,
chlorophyll,
carotenoid, proline
and activities of
defense enzymes
i.e. superoxide
dismutase (SOD),
catalase (CAT),
ascorbate
peroxidase (APX)
and phenylalanine
ammonia lyase
(PAL)
[42]
ZnO 0.1 mg ml − 1Candida albicans Inhibited the
growth
of pathogenic
C. albicans
[43]
TiO2750 mg Kg−1Rice Increase in
phosphorus content
of the plant
[44]
CeO2400 mg Kg−1Wheat Increase in
phosphorus,
potassium and iron.
Augmented amino
acids and total
sugar content
[45]
(continued)
358 M. M. M. Sharma et al.
Table 1 (continued)
Nanoparticle Application Plant
species/microbial
species
Advantage References
ZnO Clusterbean Total plant biomass
increased alongwith
enhanced
chlorophyll content
total soluble leaf
protein rhizospheric
microbial
population acid
phosphatase,
alkaline
phosphatase, and
phytase activity in
the rhizosphere
[46]
AgNPs 3000 mgl−1Cucumber Increased growth,
fruit yield, biomass,
and total soluble
solids in fruit
[47]
GNPs 10 and
80 μgml
−1 Thale cress Enhanced total
yield
[48]
Al2O350 ppm Soyabean Alleviates salinity
stress
[49]
TiO2500 mgl−1Linseed Ameliorate drought
stress damage to
plants as well as
increase in the
drought tolerance
with remarkable
improvement in
physiological
process
[50]
Even so, there is still a gap in analytical techniques that can accurately characterize
and quantify NPs in the complex environment milieu. Concurrently, the effect of
NP emission on the microbiota has grabbed escalating attention and many studies
are focusing on the mechanism of NP toxicity on beneficial microbiota. Moreover
there are multiple evidences signifying NPs as a sink for organic and inorganic co-
contaminants. Nonetheless there is still a huge void in understanding the potential
harm of NP emission in the environment [51].
It has been projected that the growing use of NPs both quantitatively and quali-
tatively will proceed to a broadening in emission sources into the environment [52].
Maximum NP containing products are coatings, paints and pigments, catalytic addi-
tives, and cosmetics [53]. Silver and titanium oxide are reported as the most used
nanomaterials in these products but 60% of the nanomaterials are still unreported.
Nanomaterials and Their Toxicity to Beneficial Soil Microbiota … 359
The ultimate fate of the NP is either soil ecosystem or aquatic ecosystem which
is independent of the product constituting the nanomaterial. NPs can enter these
bodies via three major ways: (i) discharge in the course of production of raw mate-
rial and nano-enabled products; (ii) discharge during use; and (iii) discharge during
waste handling of NP-containing products [54, 55]. NP can release in the environ-
ment directly or indirectly. Wastewater treatment plants (WWTPs) or landfills are
the sources of its direct seepage in the environment. Indirect emissions are possibly
ensuing either through the seepage of WWTPs, application of biosolids to soil, or
leachates from landfills. It has also been indicated that NP outcome in WWTPs
defines whether bare, coated, chemically or physically transformed elements are
released, and through which pathway (as effluent or biosolid) [56, 57].
The material flow method is the most accepted method to estimate the NP emission
in the environment that is based on the NP life cycle [58]. The models presume that
the NP will seep either to waste streams or directly to the soil. These emissions can
be controlled by (i) ageing or weathering, (ii) the outcome of the NP during use and
(iii) the waste management system [59–61]. Although the total production volume
could indicate towards emission of specific NP available data on production volumes
are subjective to the method of data collection used. Global approximation of NP
emissions directs that landfills (approximately 63–91%) and soils (approximately 8–
28%) obtain the major share followed by emissions into the aquatic environment and
air (7 and 1.5%, respectively, of the production bulks [62]. These evaluations permit
to identify applications with practically high environmental inference. Increase usage
of NPs in open environment can potentially raise its mass flow directly into the aquatic
and terrestrial environment [63]. For instance, NP emission from façade paints, such
as photocatalytic active amalgams, e.g. TiO2 NP, has been proved previously [64].
Additionally there are particulate emissions of anthropogenic NPs which are unin-
tentionally produced as NP. For example, particulate emissions from traffic, such as
palladium, were recognized to be in nanoscale [65]. NP remission might also be
anticipated through their direct presentation in the environment, for example, use of
iron based NPs for groundwater remediation [66] or when applying nano-pesticides
straight to agricultural fields [67]. Though some information on NP emission is
available, it is of high significance to compute their quantities and concentrations in
the environment. Quantification of NP emissions into the environment has by now,
however, been hindered by the dearth of apposite analytical techniques [68].
4 Nanoparticle Toxicity to PGPR
NPs differ in their toxicity on the basis of their type, size and origin. Their toxicity is
further governed by numerous other factors like charge, solubility and binding affinity
towards a biological site. Metal NPs and their derivatives are considered to be much
toxic with the possession of antibacterial, anticandidal, and antifungal activities [69].
In addition to their inherent toxicity, NPs also possess indirect toxicity generated as
a result of their interaction with natural organic compounds. Their interactions with
360 M. M. M. Sharma et al.
the persisting pollutants can also augment their toxicity. Furthermore, they also have
the potential to change the bioavailability of toxins [70]. The ultimate toxicity might
be the cumulative effect of protein oxidation, DNA damage, depletion of respiratory
chain protons, and generation of reactive oxygen species and induction of apoptosis.
The toxicity of nanomaterials is found to be different towards Gram positive and
Gram negative bacteria as they are known to differ in terms of the composition and
thickness of phospholipid bilayer, lipopolysaccharides and peptidoglycan in the cell
wall, thus, leading to different interactions and different level of toxicity [71]. The
bacterial community represents approximately 15% of the soil microbial community
and is a main contributor in improving plant growth in a direct or indirect manner.
The vicinity of plant roots, known as rhizosphere, is the main hub for bacterial
community. Bacteria dwelling the rhizosphere are generally termed as plant growth-
promoting rhizobacteria. The distinguished PGPR fostering plant growth belongs
to genera Rhizobium, Bradyrhizobium, Azotobacter, Bacillus, Thiobacillus, Pseu-
domonas, Azospirillum, Burkholderia, Arthrobacter, Acinetobacter, Agrobacterium,
Serratia etc. [1]. The employment of NPs in agro-ecosystems is often found to be
affecting the PGPR community, thus, ultimately affecting the plant as well as soil
health. The application of different NPs for the fulfillment of short-term goals, like to
reduce pathogen resistance and fertilizer input might end up in creating a long term
problem for the farming as well as s cientific community. The continuous application
of NPs might result in their accrual soil systems that can have long term effects on the
population of beneficial bacteria and fungi. These organisms are known to play an
important role in biogeochemical cycling of different elements, therefore, any effect
on their number might also alter the biogeochemical cycle in the environment. The
toxicity of NPs to different PGPR has been summarized in Table 2.
5 Nanoparticle Toxicity to Fungi
The antifungal activity of NPs is a well-reported phenomenon, which further warrants
their application as anti-fungal agents. In agricultural systems, the employment of
NPs is also considered as an effective alternate to control plant pathogenic fungi.
Owing to their antifungal activity, different kinds of NPs derived from Silver, Copper,
Silicon, Nickel, Magnesium, Palladium, Titanium etc. find employment as antifungal
agent in agricultural systems [93]. However, a plethora of fungi having beneficial
role towards the plant and soil also exist in the agro-ecosystems. In addition to
their role as decomposers of dead vegetation and nutrient cycling, soil fungi are also
known to safeguard the crops against different pathogenic microbes [1]. For instance,
the arbuscular mycorrhizal fungi are known to enhance the phosphate availability
to plant systems thereby acting as a key player in the maintenance of plant health
and growth. In addition, some fungi like Glomus sp. or Trichoderma sp. possess
the ability to suppress some other fungal pathogens, thus helping the plant systems
by protecting them from pathogenic attacks. Some other members belonging to the
same genus, for instance, T. asperellum, T. atroviride, T. harzianum, T. virens, and T.
Nanomaterials and Their Toxicity to Beneficial Soil Microbiota … 361
Table 2 Toxicity of different Nanoparticles towards Plant Growth Promoting Rhizobacteria
NPs PGPR Nontoxicity Remarks References
AgNPs Azotobacter vinelandii Inhibition of
nitrogenase activity
NPs induced cell damage and
apoptosis in a
dose-dependent and
size-dependent manner
[72]
AgNPs Azotobacter vinelandii and Nitrosomonas europaea Cell membrane
damage and
over-production of
Reactive Oxygen
Species
NPs led to the induction of
necrosis in A.
vinelandii and N.
europaea up to 15.20% and
42.20% respectively
[73]
AgNPs Nitrosomonas europaea Post-transcriptional
interruption of
membrane-bound
nitrifying enzyme
function, reducing
nitrification
Higher dose of NPs resulted
in disruption of cell
membrane
[74]
AgNPs Rhizobium leguminosarum,
Azotobacter chroococcum,
Arthrobacter sp,
Sinorhizobium meliloti, Serratia marcescens,
Pantoea dispersa
Growth inhibition of
PGPR
The application of AgNPs in
soil samples reduced the
abundance of three phyla
namely Proteobacteria,
Actinobacteria, and
Firmicutes by 25 to 45%
[75]
AgNPs Nitrosomonas europaea
ATCC-19718
Reduction in ammonia
oxidation and cell
death
NPs induced cell wall
damage and disintegration of
nuclei
[76]
AgNPs Rhizobium leguminosarum bv. viciae Reduction in
nodulation
NPs retarded the process of
nodulation and nitrogenase
activity
[77]
(continued)
362 M. M. M. Sharma et al.
Table 2 (continued)
NPs PGPR Nontoxicity Remarks References
ZnO and AgNPs Sinorhizobium meliloti Reduction in the length
of nodule
Below MIC, NPs treatment
led to a reduction in the nif
gene expression
[78]
CeO Bradyrhizobium japonicum Inhibition of Nitrogen
fixation
Long term exposure to NPs
can result in their
bioaccumulation in the plant
tissues
[79]
TiO2 and
Fe3O4 NPs
Soybean-unspecified rhizobia Reduction in plant
growth
NPs can influence the
colonization of the root
system by nitrogen-fixing
bacteria
[80]
TiO2 and ZnO Rhizobiales, Bradyrhizobiaceae,and Bradyrhizobium Alteration in bacterial
communities in a
dose-dependent
manner
The alteration in composition
of bacterial communities can
result in the alteration of
associated processes
[81]
CeO2 and ZnO Ensifer, Rhodospirillaceae, Clostridium, and Azotobacter Reduction in numbers
of bacteria
Alteration in the bacterial
community can change the
plant growth dynamics
[82]
TiO2, ZnO, and
Fe2O3
Rhizobium leguminosarum Reduction in nodules NP treatment altered the
symbiosis that resulted i n
reduced plant growth
[83]
ZnO R. leguminosarum bv. viciae 3841 Damage to the
bacterial surface
NPs disrupted the
Rhizobium–legume
symbiosis that resulted i n
reduced plant growth and
productivity
[84]
(continued)
Nanomaterials and Their Toxicity to Beneficial Soil Microbiota … 363
Table 2 (continued)
NPs PGPR Nontoxicity Remarks References
Molybdenum
(Mo)-based
nanomaterials
Soybean-unspecified rhizobia Reduction in the
nitrogen fixation
capacity of the
soybean–rhizobia
symbiotic system
Alteration in symbiosis led to
a significant change in the
agronomical and
physiological parameters in
soybean
[85]
TiO2Rhizobium trifolii Reduction in growth
rate of Rhizobium
trifolii
Impaired symbiosis reduced
the shoot length of red clover
by 41 to 62%
[40]
Ag, CuO and ZnO Pseudomonas putida KT2440 NP treatment resulted
in cell death
The off-target effect of
different NPs can result in
death of beneficial bacteria
[86, 87]
Graphene Oxide
NPs
Bacillus marisflavi, Bacillus cereus, Bacillus
subtilis, Bacillus megaterium, and Bacillus mycoides
Reduction in cell
viability
NP mediated reduction i n
PGPR numbers can affect the
plant growth and health
[88]
Al2O3Pseudomonas fluorescens, Bacillus megaterium, Bacillus
brevis, and Azotobacter vinelandii
Increased in cell death NP treatment led to a
decrease in microbial
population of the soil,
leading to decrease in
available forms of nutrients
[89]
ZrO2 (Zirconia)
and TiO2
B. megaterium, P. fluorescens, A. vinelandii and B. brevis Growth inhibition The toxicity of NPs was
governed by the size,
hydrophobic potential and
zeta potential
[90]
AgNPs Maize rhizosphere associated PGPR Reduction in
enzymatic activity
NP treatment altered the
rhizosphere associated
bacterial community that
further affected the carbon
dynamics
[91]
(continued)
Nanomaterials and Their Toxicity to Beneficial Soil Microbiota … 365
viride are also reported as effective bio-stimulants often used for horticultural crops
[94, 95]. The exposure of NPs to different fungi has been reported differentially
by different researchers, some claim it as beneficial whereas other claiming it as
totally detrimental to the growth of fungi. However, it is always clear that increasing
concentrations of any NP are always toxic as they penetrate the fungal hyphae and
damage their innate morphological features. The repeated application of NPs in field
conditions, can lead to their accrual in the soil systems, and the annual concentra-
tion of NPs will keep on increasing with each crop cycle. Thereby, the repeated
foliar or soil application might keep on increasing their concentration, in turn their
toxicity, to the beneficial fungi. Although, this view requires long-term studies, that
are currently lacking, but it also seems to be more realistic and practical. The toxi-
cological attributes of different types of NPs, as reported in literature, have been
summarized in Table 3.
6 Mechanism of Nanoparticle Toxicity
The NPs used in bio systems should be in safe regarding their mode of action and
their compatibility with the cells and nucleic acids should be paramount. Different
adverse effects of the use of NPs can result in the form of cytotoxicity, genotoxicity
and immunogenicity [107].
6.1 Cytotoxicity
Cytotoxicity is considered as one of the most relevant factors while using the NPs for
applications in bio-systems. For instance, when they are used in f orm of drug or gene
delivery carriers, because of their small size they can reach up to sensitive organs
and can also influence them adversely [108]. One of the prominent mechanism of
the cellular toxicity of the NPs is governed by the incredibly high surface are to
volume ratio which tends to production of reactive oxygen species (ROS) in the host
cells and tissues. These ROS are responsible for damaging the cell membrane, DNA
and protein and ultimately leads to the death of cell [109]. For instance, the NPs
can activate the redox system by rendering the immune cells like neutrophils and
macrophages to induce ROS directly [110]. Apart from the surface area of the NPs
the particle surface charge is also a determinant of the cytotoxicity deciphered by the
NPs. The high positive charge of the NPs tends to have intensive electrostatic inter-
action with the cell. For example, in a study conducted on the A549 cells using ZnO
NPs with different shape and size but possessing different charge, it was observed that
the positively charged NPs were more cytotoxic than negatively charged NPs [111].
High electrostatic interaction also leads to the increased uptake of the NPs by the
cells which may cross the threshold level of uptake as the tissues safely uptake 0.7%
of the applied dose and beyond which, it can be detrimental to cells and tissues [112].
366 M. M. M. Sharma et al.
Table 3 List of nanoparticles reported for biocidal activity against different plant-beneficial fungi
Nanoparticle Application/concentration Plant species/microbiota Nanotoxicity References
AgNPs 50 mg Kg−1Soil microbiota Reduced biological activity in soil and
impacted the fungal community
structures, negative impact on nitrogen
cyclinginsoil
[96]
AgNPs 800 μgKg
−1Faba bean Stunted the process of mycorrhizal
colonization, mycorrhizal responsiveness
and glomalin content. Modifications in
the intracellular deterioration of
cytoplasmic components by means of
autophagy
[77]
AgNPs 2.5mgKg
−1Maize A significant decrease in the growth and
diversity of AM fungi and remarkable
variation in their structure. Deterioration
of the mutual interaction between plants
and AM fungi and negatively influence
the rhizospheric soil P cycling
[97]
AgNMs White rot fungi Significantly inhibited the growth of
white rot fungi with effects on the
chemical composition of mycelia
[98]
Multiwalled carbon
nanotubes (MWNTs)
10,000 mg Kg−1Soil microbiota Alteration in fungal community dynamics [99]
Nanosized zero-valent
iron (nZVI)
Arbuscular mycorrhizal fungi Potential reduction of arbuscular
mycorrhizal fungi
[100]
Single-walled carbon
nanotubes (SWCNTs)
1mgg
− 1Soil microbiota Decrease in total beneficial soil
microbiota
[101]
TiO2NPs 250 μgml
−1S. cerevisiae Impacts the cell viability of the yeast [102]
(continued)
Nanomaterials and Their Toxicity to Beneficial Soil Microbiota … 367
Table 3 (continued)
Nanoparticle Application/concentration Plant species/microbiota Nanotoxicity References
Citrate-AgNPs Phanerochaete chrysosporium Diminution in the activities of four
dehydrogenases synthesized in the fungus
mycelium
[103]
CoNPs 10–4 parts by weight Trichoderma asperellum Inhibits hyphal growth [104]
AgNPs 200 ppm T. harzianum DNA fragmentation [105]
AgNPs 120 ppm Trichoderma viridae Growth inhibition [106]
368 M. M. M. Sharma et al.
Additionally, the abundance of negatively charged macromolecules Glycosamino-
glycans on the cell membrane tends to interact more with the positively charged NPs
[113]. The shape of the NPs has also been found to contribute to their cytotoxicity.
[114] found that the rod shaped Fe2O3 NPs had more cytotoxic effect as compared to
spherical NPs n a murine macrophage cell line (RAW 264.7). The phenomenon by
which NPs offer cytotoxicity is called prooxidation, which means either production
of ROS or suppression of antioxidants, or both. Apart from the production of ROS
the negatively altered levels of antioxidants like α-tocopherol and GSH which leads
to the injury or death of the cell [115]. Another parameter which determine the cyto-
toxicity of any substance is the depolarization, which refers to the decrease in the cell
membrane’s potential and is considered as the initial signs of the cytotoxicity. One
such instance is the depolarization of the cell membrane of human bronchoalveolar
carcinoma-derived cells (A549) when treated with different size of Al2O3,CeO
2 and
TiO2 NPs [116]. The cytotoxicity of NPs is also indicated by the trepidation of intra-
cellular calcium in homeostasis, which is concomitant with the energetic discrepancy
and the cellular dysfunction [117]. For example, sphere-shape silica NPs exhibited
size-related toxicity and calcium ions imbalance in the neuronal cells [118]. Recently,
it has been demonstrated that the NPs can also initiate the autophagy in host cells and
that can lead to death of the healthy cells [119]. Some NPs which exhibit cytotoxicity
reduce the mitochondrial membrane potential. The reduction in membrane potential
can lead to the rupture or disruption of the cell organelle and can lead to apoptosis.
For instance, the grapheme oxide NPs when exposed to Leydig (TM3) and Sertoli
(TM4) cells, a significant reduction in MMP were observed which lead to the cyto-
toxical response from the cells [120]. Furthermore, NPs can cause some irreversible
changes to the structural proteins of the cells and also denature them which may
result in the cell injury. One such example is the denaturation of haemoglobin after
exposure to the titanium oxide NPs [121]. NPs also exhibit cytotoxicity by arresting
the cell cycle. Cells undergoing the cell cycle arrest will either die or survives with
the conceded function. For instance the Titanium dioxide NPs were used to arrest
the G1 cell cycle in the cancer cells [122].
6.2 Genotoxicity
Genotoxicity is the ability of the chemicals to alter the genetic material of the host cell,
which can be evaluated by observing different kind of genetical damage such as DNA
damage, chromosomal aberrations and genetic mutation. Genotoxicity is exhibited
by NPs either in two ways, classified as the primary genotoxicity in which the NPs
shows genotoxic effects without inflammation and secondary genotoxicity accounts
by the production of ROS due to particle inflammation [123]. The oxidative stress
induced by NPs can result in the DNA damage which may can lead to the abnormal
growth of cell and can possibly lead to carcinogenesis and fibrogenesis [124]. For
instance, the DNA breakage and repair and the activation of signalling pathways
were observed in the human mesothelial cells after exposure to carbon nanotubes
Nanomaterials and Their Toxicity to Beneficial Soil Microbiota … 369
[125]. Alongside, DNA damage the NPs can introduce genetic instability in the host
cells. For example, [126] tested the in vivo activity of Titanium dioxide NPs in mice
and reported the presence of high 8-hydroxy-2'-deoxyguanosine (8-OHdG) in the
treated cells, which is an indicative of DNA damage, additionally, the prevalence
of γ-H2AX foci was also noticed, which shows the double-strand breaks in DNA.
The genotoxicity of NPs is also determined by the application dose. For example,
Titanium dioxide NPs were found to be genotoxic above 1.25 mM in Allium cepa
and human lymphocytes [127]. In a recent study, Zinc oxide NPs found to be geno-
toxic to Deinococcus radiodurans where the high dose of NPs downregulated the
genes related to DNA repair cascade [128]. Chromosome break, chromosome stick-
ness and brigge, acentric fragments, translocations, gaps and micronuclei formation
are the predominant forms of chromosomal aberrations observed in NPs treatments
[129]. For instance, the silver NPs when tested upon Nicotiana tabacum and Swiss
albino male mice the host cells showed chromosomal aberration in a dose-dependent
manner [130]. In another report it was observed that the iron-oxide NPs when tested
in vivo in wistar rats, caused different kind of chromosomal aberration to the host
cells such as chromosome breaks, chromatid breaks, acentric fragments, dicentric
chromosomes, and chromosomal rings and the damage was directly proportional
to the concentration of NPs used in the study [131]. Genetic mutations are also
accompanied by the t oxicity of NPs, which may result in detrimental consquences
like cell of death or the abnormality in growth. For instance, in vitro genetotoxicity
assays revelaed the genetic mutations in the embryonic fibroblasts of mouse when
exposed to the amorphous silica NPs [132]. Apart from the genetic mutations, chro-
mosomal aberration and DNA damage NPs can also alter the expression of some
genes, which can be detrimental to the function of those cells or tissue inside the
body. For instance, Mesoporous silica NPs, when tested with the human embryonic
kidney 293 (HEK293), found to modify the expression of around 1800 genes, which
might trigger cellular dysfunction or certain benign diseases [133].
6.3 Immunogenecity
The uptake of NPs by the cells is followed by the cellular and humoral response or
in the form of antibodies from the cells leads to immunogenicity [134]. Immuno-
genicity can lead to immunogenic cell death, which is generally used in tumor-
treatment therapy to not only kill the cancer cells but also to induce antitumor immune
response. Apart from that the NPs can undesirably interact with the macrophages in
the form of immunosuppression and immunostimulation and can therefore lead to
the autoimmune disorders [135]. The ultimate operational purpose of the immune
system is to protect the host from alien substances and if the NPs are recognized
inadvertently, they can be toxic to host and can lead to further complications such
as formation of granuloma in animal cells after exposure to carbon nanotubes [136].
The immunogenicity of NPs is also associated with the type of charge carried by
them. Positively charged NPs tends to have more inflammatory reaction from the
370 M. M. M. Sharma et al.
host as compared to negatively charged particles [137]. For example, Schanen et al.
[138] tested Titanium dioxide NP in an in vivo human immune setup and findings
suggested that the NPs notably provoked the inflammation [138]. On the molecular
level the cytokines are the essential compounds required for mediating an immune
response, however they are also considered as the marker of immunotoxicity and has
been used as an indicative for detecting the immunogenicity and immunotoxicity of
the NPs [139]. It is also believed that the hydrophobicity of the NPs also plays an
important role in deciding the immune response from the host. For instance, when
gold NPs were tested against the mouse cells, the gene expression profile of the
cytokines were found to be increased with the upsurge in hydrophobicity [140]. In
another study conducted on Palladium NPs against the wistar rats it was observed
that the cytokine serum level were modulated upon exposure to the NPs [141]. The
immunogenicity of NP is being studied widely to use as an adjuvant as to improve the
anteginicity of the conjugated weak antigen. Recently, the lipid squalene NP has been
used as an adjuvant to enhance the immunogenicity of SARS-CoV-2 spike subunit
protein [142]. Lately, the immunogenic potential of NPs has been explored to combat
lethal diseases like cancer. The immunogenic cell death (ICD) by NP application has
been explored for their use in cancer immunotherapy [143]. The ICD by the NPs
stimuli has shown to generate an active immune response in the body via discharge
of danger-associated molecular patterns (DAMPs) in the tumor environment [144].
A no. of ICd inducers has been developed till date and they are being used alone
or in combination with other therapies [145]. Additionally the, nanocarrier based
drug delivery systems are also being used as a combination therapy plus ICD elicitor
[146].
7 Effect of Nanoparticle Toxicity on Fungi and Bacteria
The fungi and bacteria are the inseparable part of the ecosystem and play a very impor-
tant role in the energy cycling, decomposition of the dead and waste material, and
nutrient uptake by the plants and circulation of the nutrition in the ecosystem [147–
150]. The NPs have been implied to plant rhizosphere for the better uptake of minerals
to improve their overall productivity, however the applied NPs can be threating to
the microbiota of the root zone which further depends upon a number of factor like,
the type of microflora, the texture of soil and the, organic matter content, immo-
bilization and deposition of NPs [1]. Like any other living cell, the bacterial and
fungal cells are also negatively influenced by the NPs after a threshold concentra-
tion and the ROS cascade is trigged in a similar fashion in these cells. For instance,
Gold NPs of different shapes were examined on the four common and widespread
types of fungus namely Aspergillus niger, Mucor hiemalis, and Penicillium chryso-
genum and it was observed that the NPs were toxic to all type of fungus to some
extent and the toxicity was largely carried by larger and non-spherical NPs [151].
The toxicity exerted by the NPs can have different secondary effects depending upon
the characterstics of the NPs and the host cells. For instance the Zinc oxide NPs of
Nanomaterials and Their Toxicity to Beneficial Soil Microbiota … 371
lower than 100 nm caused injury to the cell wall and adversely affected the repro-
ductive configurations of Mycena citricolor and Colletotrichum sp [152]. In another
study conducted in Aspergillus flavus, the MoO3 NPs significantly hampered the
growth, persuaded the nuclear contestation, distorted the hyphae morphology and
ultimately caused the death of cell [153]. Apart from the aforementioned causes of
the cell death or injury mediated by the NPs to the host cells, the NPs can also impair
the metabolic functioning of the cells, which may result in irreversible damage. For
example, nanodiampds of size 3.4 nm when applied to the Phanerochaete chrysospo-
rium, the manganese peroxidase and laccase activity were subdued which resulted
in harm of cytoplasm and devastation of mycelium [154].
The interaction of NPs with bacteria and fungi can also be toxic and can cause
severe damage to the cells resulting in their death (Fig. 2). The NPs can cause the
extensive damage to the cell wall by squandering the potential of plasma membrane
and can also render diminution of ATP [155]. For instance, the mechanical damage
in the bacteria were caused by the toxic anti-bacterial properties of carbon-nanotubes
[156]. Additionally, the toxicity shed by the NP and also reduce the bio-functional
properties of the bacteria such as biological nitrogen fixation. For instance, the silver
NPs studied on the soil bacteria Azotobacter vinelandii, the toxic effects of NPs dras-
tically reduced the number of cells and induced apoptosis in the 1/5th of the popu-
lation and also reduced the biological nitrogen fixation significantly [72]. Similar
to the fungal cells reaction t o the NP toxicity, metabolism of bacteria can also be
hampered by the NP toxicity. For instance, CuO NPs when tested against the sulfate
reducing bacterium Desulfovibrio vulgaris, the CuO NPs largely downregulated the
genes involved in electron transfer and respiration [157]. Additionaly, when the CuO
NPs activity were tested on the soil nitrifying bacteria, the NP toxicity tend to subdue
the nitrification kinetics [158].
8 Conclusion and Future Prospects
The agricultural sector is facing a lot of challenges, for instance, reduced crop
production, increasing incidence of different biotic and abiotic stresses, reduced
soil health and continuously changing climatic conditions. Plants, being sessile,
have to face all the stresses and ultimately their growth and productivity gets irre-
versibly affected. The challenge of sustainably enhancing the agricultural produc-
tivity brought in several nano-enabled tools, like, Nano fertilizers, nano pesticides,
nano herbicides, nano sensors etc. To fulfill the nutritional demands of plant systems,
several metal and their derivative NPs are also applied either via foliar spray or
by soil application. Initially, the sudden increase in the yield and a sharp decline
in the pathogen attacks due to nano-technological, that too, in an economical way
excited the researchers. However, their inherent possession of toxic attributes towards
plant-beneficial rhizosphere-inhabiting microbiota has again put a question on the
agricultural sustainability. The long term usage of NPs leads to their accrual in the
soil systems and may lead to permanent alteration in the population dynamics of
372 M. M. M. Sharma et al.
Fig. 2 A portrayal showing NP emission into agricultural environment and the potential toxicities
to soil microbiota inhabiting plant rhizosphere
plant-beneficial microbiota. Plants have evolved in a world of microbes, therefore,
alteration in the evolutionary-selected microbial symbionts can irreversibly damage
their health and food quality. Furthermore, tracking NPs in the environment upon
their release seems to be an impossible task. Therefore, a clear assessment of their
off-target effects and toxicological attributes towards, beneficial microbiota is the
need of hour. In addition, their persistence and half life time in the environment
should also be evaluated before their application in the agricultural systems.
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