Download as pdf or txt
Download as pdf or txt
You are on page 1of 21

Environmental Science and Pollution Research (2024) 31:40224–40244

https://doi.org/10.1007/s11356-023-30556-y

SPECIAL ADSORBENT MATERIALS FOR RETENTION AND DEGRADATION


OF POLLUTANTS FROM FLUID PHASES

Recent advances and mechanisms of microbial bioremediation


of nickel from wastewater
Sonu Sharma1 · Monu Sharma1 · Raman Kumar1 · Mohammad Sayeed Akhtar2 · Ahmad Umar3,4 ·
Abdulrab Ahmed M. Alkhanjaf5 · Sotirios Baskoutas6

Received: 22 February 2023 / Accepted: 16 October 2023 / Published online: 6 November 2023
© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2023

Abstract
The global concern over emerging pollutants, characterized by their low concentrations and high toxicity, necessitates effec-
tive remediation strategies. Among these pollutants, pharmaceutical and personal care products, pesticides, surfactants,
and persistent organic pollutants have gained significant attention. These contaminants are extensively distributed within
aquatic ecosystems, posing threats to both human and aquatic physiological systems. Nickel, a valuable metal renowned
for its corrosion-resistant properties, is widely utilized in various industrial processes, leading to the generation of nickel-
containing waste streams, including batteries, catalysts, wastewater, and electrolyte bleed-off. Contamination of soil, water,
or air by these waste materials can have adverse effects on the environment and human health. This review article focuses
on the recent advancements in environmental and economic implications associated with the removal of nickel from diverse
waste sources. Physicochemical technologies employed for treating different nickel-containing effluents and wastewater are
discussed, alongside bioremediation techniques and the underlying mechanisms by which microorganisms facilitate nickel
removal. The recovery of nickel from waste materials holds paramount importance not only from an economic standpoint
but also to mitigate environmental impacts.

Keywords Emerging pollutants · Pesticides · Surfactants · Nickel · Wastewater · Physico-chemical techniques ·


Bioremediation

Abbreviations
DDT Dichlorodiphenyltrichloroethane
Responsible Editor: Robert Duran AS Activated sludge
MBR Membrane bioreactor
* Raman Kumar
ramankumar4@gmail.com SMBR Submerged membrane bioreactor
HMs Heavy metals
1
Department of Biosciences and Technology, ACC​ 1-Aminocyclopropane-1-carboxylic acid (ACC)
Maharishi Markandeshwar (Deemed to be University), deaminase
Mullana (Ambala), Haryana 133207, India
IAA Indole-3-acetic acid
2
Department of Botany, Gandhi Faiz-e-Aam College, RBC Rotating biological contractor
Shahjahanpur, Uttar Pradesh 242001, India
PGPB Plant growth-promoting bacteria
3
Department of Chemistry, Faculty of Science and Arts,
and Promising Centre for Sensors and Electronic Devices
(PCSED), Najran University, Najran 11001, Saudi Arabia
4
Introduction
Department of Materials Science and Engineering, The Ohio
State University, Columbus, OH 43210, USA
5
Environmental contamination is a global concern for
Department of Clinical Laboratory Sciences, College
of Applied Medical Sciences, Najran University,
ecotoxicologists, environmental biologists, biochemists,
Najran 11001, Saudi Arabia pathologists, and other specialists. Metal-polluted wastes
6
Department of Materials Science, University of Patras,
have become a laborious issue of significant environmental
26500 Patras, Greece significance (Lim et al. 2008; Zhou et al. 2023; Daź et al.

13
Vol:.(1234567890)
Environmental Science and Pollution Research (2024) 31:40224–40244 40225

2022; Yang et al. 2023). Water contamination is caused by a While plants and animals require small amounts of nickel
wide range of contaminants, including dangerous heavy met- for various physiological functions, elevated levels can have
als and emerging toxic compounds (Wang 2023; Yin et al. detrimental effects. Plants experience disrupted metabolic
2019; Shen et al. 2023; Gong et al. 2020; Priya et al. 2022; activities, growth disturbances, abnormal flowering, and
Ren et al. 2023). Among these contaminants, heavy metals, decreased biomass production (Ahmad and Ashraf 2011).
with their wide sources, long residual time, and difficulty in Animals exposed to nickel face risks such as cancer, respira-
degradation, pose a significant threat to marine ecosystems tory illnesses, allergies, cardiovascular diseases, and renal
(Jin et al. 2022; Diab et al. 2020; Yang et al. 2022; Wang disorders due to mitochondrial disorders and oxidative stress
et al. 2022). The increased frequency of human activities, induced by nickel (Genchi et al. 2020). The interference of
driven by industrialization, has led to a surge in heavy metal heavy metals like nickel with normal biological processes
pollution, particularly the pollution caused by heavy metal in human organs poses severe health risks (Acosta et al.
ions (HMIs) (Zeng et al. 2022; Huang et al. 2018; Li et al. 2018; Das et al. 2021; Renu et al. 2021) (Fig. 1).
2022). This pollution extends to natural resources such as Given the persistence of nickel contamination and its
water and land, which are crucial for agriculture and soci- detrimental effects, effective techniques for the removal
etal well-being but have suffered substantial damage from of nickel from wastewater are crucial. Bioremediation,
human activities (Akhtar et al. 2018; Niyonzima et al. 2023; utilizing microorganisms, has emerged as a cost-effective
Masindi and Muedi 2018). and environmentally favorable strategy for the removal of
Certain HMIs have been found to be hazardous at concen- heavy metals, including nickel, from contaminated environ-
trations as low as 0.001–0.1 ppm, posing a serious threat to ments. Understanding the recent advances and mechanisms
human health (Verma and Kuila 2019; Gao et al. 2022; Chen of microbial bioremediation for nickel removal from waste-
et al. 2020; Suo et al. 2022). Nickel, a transition metal, is water is essential for developing efficient and sustainable
considered a heavy metal due to its physiological necessity remediation strategies.
at low concentrations but harmful effects at higher concen- Nickel (Ni) is a remarkable metal that was discovered
trations (Engwa et al. 2019; Kour et al. 2019). Nickel con- by Axel Fredrik Cronstedt in 1751. With its beautiful, sil-
tamination has emerged as a significant environmental issue, very-white appearance, nickel is the 28th element on the
especially in industrial wastewater discharges, as nickel is periodic chart and accounts for approximately 1% of the
non-biodegradable and can accumulate in organisms (Lu and Earth’s crust (Lenntech Water Treatment and air purifica-
Astruc 2018; Burakov et al. 2018; Kour et al. 2019). Sec- tion 1998). It possesses unique physical and chemical prop-
tors such as mining, metallurgy, electroplating, tanning, and erties, including magnetizability, a high melting point of
others release substantial amounts of potentially hazardous 1453 °C, exceptional corrosion and oxidation resistance,
heavy metals, including nickel (Liu and Lu 2022; Burakov low thermal and electrical conductivities, and resilience to
et al. 2018; Kour et al. 2019; Abdullah et al. 2023). extreme temperatures. Nickel’s atomic number is 28, and its

Fig. 1  Illustration of the path-


way of nickel contamination in
the food chain and its impact on
the human health

13
40226 Environmental Science and Pollution Research (2024) 31:40224–40244

electron configuration is 1­ s2, ­2s2, ­2p6, ­3s2, ­3p6, ­4s2, ­3d8, with mg/L in drinking water. Exposure to nickel has been associ-
an atomic mass of 58.71 (Marin 2022). ated with kidney damage, lung fibrosis, skin rashes, and can-
Nickel commonly crystallizes as a face-centered cubic cer. Divalent nickel, in particular, has been linked to lung,
lattice and is the strongest, most malleable, and abundant bone, and nasal cancers (Fig. 2).
component of the Earth’s crust. In aqueous solutions, nickel Ni compounds are recognized as potent carcinogens capa-
primarily exists in the Ni(II) oxidation state. Through alloy- ble of inducing rapid cell alterations and tumor formation
ing with other metals, nickel enhances their durability and in both humans and animals. High levels of Ni(II) exposure
provides protection against corrosion across a wide range have been correlated with an increased risk of lung cancer
of temperatures (Marin 2022). It exhibits ferromagnetic and pleomorphic cancer. These metallic species have also
properties at room temperature, but also exists in a non- been reported to cause genetic defects and toxic effects on
ferromagnetic hexagonal form. Ullmann’s Encyclopaedia of cells. Heavy metals like nickel can influence cell signaling
Industrial Chemistry provides comprehensive information pathways, including G protein-coupled receptors, MAP
on nickel’s physical and chemical characteristics, as well as kinase, and nuclear transcription (Rodríguez and Quesada
its occurrence, extraction, purification methods, compounds, 2006). Excessive concentrations of nickel have been asso-
and alloys. Nickel compounds and alloys find extensive ciated with cardiovascular and kidney diseases, as well
applications in various industrial and commercial sectors as cancer (Islam et al. 2019). Ni(II) is harmful to various
(Coman et al. 2013). organisms, affecting the growth and development of plants,
Nickel is widely used in the production of stainless steel, animals, and microbes. It induces oxidative stress, leading
non-ferrous alloys, and nickel-based superalloys known for to oxidative and non-oxidative damage to cell membranes,
their excellent corrosion and temperature resistance. Indus- proteins, lipids, and DNA (Das et al. 2008a; Barrera-Díaz
tries such as machinery manufacturing and precision elec- et al. 2012). The toxicity of nickel at the cellular level can be
tronics heavily rely on nickel alloys. Additionally, nickel examined through techniques such as scanning and transmis-
compounds and complexes serve as efficient catalysts in sion electron microscopy.
numerous syntheses, while nickel oxide hydroxide is com- Considering the extensive usage of nickel and the associ-
monly employed in Ni-based rechargeable batteries (Coman ated health and environmental concerns, effective methods
et al. 2013). Divalent nickel is extensively utilized in mineral for the remediation of nickel contamination are impera-
processing, metal finishing, electroplating, battery manufac- tive. Microbial bioremediation has emerged as a promising
turing, leather tanning, zinc base casting, and hydrometal- approach for the removal of nickel from wastewater. Under-
lurgical industries. Its applications span from magnets to standing the recent advances and mechanisms involved in
specific alloys and stainless steel. microbial bioremediation can contribute to the development
However, despite its widespread use, nickel and its com- of efficient and sustainable strategies for addressing nickel
pounds pose significant health risks. The World Health pollution.
Organization (WHO) guidelines specify a maximum allow- Excessive accumulation of nickel in plants can have detri-
able level of 3 mg/L for Ni(II) in sewage and a limit of 0.02 mental effects on their growth and development. High levels

Fig. 2  Comprehensive illustra-


tion of the adverse human
health effects caused by nickel
exposure

13
Environmental Science and Pollution Research (2024) 31:40224–40244 40227

of nickel can slow down the growth of shoots and roots, can be utilized as well. Adsorption using activated carbon
affect branch development, and alter the shape of various and the investigation of heavy metal biosorption in multime-
plant parts. It can also lead to abnormal flowers, reduced tallic systems have shown promising results in the removal
biomass production, leaf spotting, and disruption of mitotic of heavy metals from wastewater (Borja et al. 2016; Efome
root tips. Nickel toxicity can result in iron deficiency, caus- et al. 2019; Qiu and He 2019; Liu et al. 2020; da Silva
ing chlorosis (yellowing of leaves) and foliar necrosis (death Oliveira et al. 2007; Pang et al. 2011; Dong et al. 2022; Sun
of leaf tissue) (Fig. 3). et al. 2018; Dhandole et al. 2020; Shi et al. 2018; Li et al.
Metabolic functions, cell wall flexibility, cell divisions, 2018; Ding et al. 2020; Gapusan and Balela 2020; Topare
and hydrolytic enzyme activities are all reduced under nickel and Wadgaonkar 2022; Verma and Balomajumder 2020;
toxicity, which can negatively impact seed germination and Aloulou et al. 2020; Azimi et al. 2017; Semerjian 2018; de
seedling development. Protein synthesis and the movement Sa Costa et al. 2021; Bai et al. 2022). These techniques aim
of stored food from the endosperm to the developing embryo to reduce nickel and other heavy metals to simpler forms or
can be disturbed, leading to a loss of seed germination and immobilize them for safe disposal or reuse.
seedling development. Root growth is particularly affected Bioremediation is a widely documented technique for the
by nickel toxicity (Tang et al. 2022a; Seregin et al. 2003; removal of heavy metals and organic pollution, known for its
Seregin and Kozhevnikova 2006; Shaikh et al. 2022; Walker cost-effectiveness and environmental friendliness (Dönmez
et al. 1985; Bishnoi et al. 1993). and Aksu 2001; Costa et al. 2022; Tang et al. 2022b). Vari-
Nickel toxicity also interferes with plant metabolism, pre- ous organisms, including bacteria, yeast, fungi, algae, and
venting proper transpiration and photosynthesis. It can alter plants, have been found to be effective agents in bioremedia-
the ultrastructure of plants and lead to decreased yields in tion (Fig. 4, Tables 1, 2, and 3). Biosorption, a process where
crops. Increased levels of nickel significantly inhibit seed bio-derived products or waste materials are used as adsor-
germination and seedling development in various plant spe- bents, plays a crucial role in bioremediation. The adsorp-
cies. Higher concentrations of nickel reduce water content tion technique is simple and cost-effective for the separation
in both dicot and monocot plants, further contributing to the and recovery of metal ions from aqueous solutions (Li et al.
toxicity effects. The suppression of protein and chlorophyll 2018; Molina-Campos et al. 2020; Bawazeer 2022).
processes is closely associated with nickel toxicity in plants The functional groups present on the surface of bioad-
(Zhang et al. 2007; Rao and Sresty 2000; Naz et al. 2022). sorbents are primarily responsible for pollutant removal
To address nickel contamination in wastewater, several in the biosorption process. Studies by Wong et al. (2018),
techniques are available for preconcentration and removal of Georgieva et al. (2020), and Qu et al. (2021) have success-
Ni(II). These include membrane filtration, biological treat- fully removed Ni(II) and other contaminants using various
ment, chemical coagulation and flocculation, solvent extrac- bioadsorbents such as charcoal, sawdust, straw, dried fun-
tion, photocatalytic degradation, and adsorption. Adsorption gal, bacterial, algal, and plant biomass. Parameters such as
is one of the most commonly used methods for removing pH, initial pollutant concentration, temperature, and surface
heavy metal ions from wastewater, including nickel. Other characteristics of the bioadsorbent, including functional
physicochemical techniques such as ion exchange, precipita- groups, significantly influence pollutant biosorption.
tion, reverse osmosis, electrochemical treatment, and mem- Bioremediation is a biotechnological approach used
brane technologies are also employed. Biological methods to remove or treat contaminants. It involves the use of

Fig. 3  Visual depiction of the


diverse adverse effects on plants
from nickel exposure

13
40228 Environmental Science and Pollution Research (2024) 31:40224–40244

Fig. 4  Diverse microorganisms


utilized in bioremediation for
environmental cleanup

Table 1  Different bacterial species, removal rates, and mechanisms for metal removal in wastewater treatment
Bacteria Removal rate Associated mechanism References

Bacillus megaterium 1295S 80.46% Accumulation and surface sorption Gheethi et al. (2017)
Bacillus aryabhattai HU-39 89% Accumulation and surface sorption Khadim et al. (2019)
Klebsiella sp. USL2S 86.06% Biosorption Orji et al. (2021)
Desulfovibrio desulfuricans 90.1mg/g Biosorption Kim et al. (2015)
Pseudomonas aeruginosa 8.26mg/g Biosorption Kang et al. (2005)
Micrococcus spp. 90% Sulaymon et al. (2013)
Pseudomonas flurescens 4F39 80% López et al. (2002)
Streptomyces noursei 0.79 mg/g Biosorption Mattuschka and Straube (1993)
Microbacteriumsp. MRS-1 95% Sathyavathi et al. (2014)
B. thuringiensis 15.7% Biosorption Öztürk (2007)
Escherichia hermannii 130.57 mg/g Biosorption Hernandez-Cruz et al. (1998)
Enterobacter cloacae 117.12mg/g Biosorption Hernandez-Cruz et al. (1998)
Acinetobacter baumannii 8.8mg/g Biosorption Rodríguez and Quesada (2006)
Yarrowia lipolytica 138.9mg/g Biosorption Shinde et al. (2012)
Stenotrophomonas maltophilia 54.3 mg/g Biosorption Wierzba (2015)
Oedogonium hatei 40.9 mg/g Biosorption Gupta et al. (2010)
C. vulgaris 60.2% Biosorption Aksu et al. (2002)
E. hermannii 175.12% Biosorption Hernandez-Cruz et al. (1998)
B. infantis 42% Bioaccumulation Beglari et al. (2022)

organisms to eliminate or utilize pollutants in a polluted in biodegradation in various polluted environments (El-
environment. Bioremediation is considered a safe, cost- Sheekh et al. 2015).
effective, and eco-friendly method for removing toxins Biosorption, on the other hand, differs from biore-
from contaminated water (Salgot and Folch 2018). It can mediation as it involves living organisms accumulating,
be performed in situ (at the contaminated site) or ex situ decomposing, mineralizing, transforming, and sorbing pol-
(outside the contaminated site) and includes techniques lutants through functional groups on their cell surfaces.
such as bioreactor suspension, phytoremediation, bioleach- Different enzyme-catalyzed mechanisms are responsible
ing, biostimulation, and composting. Active members for the degradation, mineralization, and transformation of
of microbial consortia, including Nitrosomonas, Pseu- pollutants into less hazardous forms, such as carbon diox-
domonas, Penicillium, Bacillus, Xanthobacter, Flavo- ide, methane, water, and biomass (Han et al. 2020). Heavy
bacterium, and Mycobacterium, play significant roles metals and certain recalcitrant organic compounds, like

13
Environmental Science and Pollution Research (2024) 31:40224–40244 40229

Table 2  Fungal species, removal rates, and mechanisms for metal removal in wastewater treatment
Fungi Removal rate Associated mechanism References

Phanerochaete chrysosporium 89.4% Adsorption by surface functional group Noormohamadi et al. (2019)
Trichoderma harzianum 11000 mg/kg Accumulation inside mycelia Cecchi et al. (2017)
Aspergillus flavus CR500 73.1% Accumulation inside mycelia and biosorption Kumar and Dwivedi (2020)
on mycelia
Trichoderma asperellum TS141 78% Accumulation inside the mycelia Hoseinzadeh et al. (2017)
Phlebia brevispora 72·7% Sharma et al. (2022)
Penicillium sp. MRF1 74.6% biosorption Sundararaju et al. (2020)
Aspergillus versicolor 30.05% Bioaccumulation Taştan et al. (2010)
Trichoderma aureoviride 88% Biosorption Siddiquee et al. (2013)
Fusarium flocciferum 5.2/100 mg Biosorption Delgado et al. (1998)
Trichoderma virens T128 Biosorption Siddiquee et al. (2013)
Trichoderma harzianum T32 835.1 mg/g Biosorption Siddiquee et al. (2013)
Phanerochaete chrysosporium (ATTC 101.34 mg/g Biosorption Iqbal and Saeed (2007)
24725)
Trametes pubescens MB 89 8.6% Biosorption Enayatizamir et al. (2020)

Table 3  Algal species, removal Algae Removal rate Associated mechanism References
rates, and mechanisms for metal
removal in wastewater treatment Dunaliella sp. 80.8% Bioaccumulation and Dahmen-Ben Moussa et al. (2018)
binding on cell surface
Asparagopsis armata 17.7mg/g Biosorption Romera et al. (2007)
Codium vermilara 13.2mg/g Biosorption Romera et al. (2007)
Durvillaea antarctica 32.8mg/g Biosorption Guarín-Romero et al. (2019)
Cystoseria indica 18.17mg/g Biosorption Khajavian et al. (2019)
Oedogonium westi 59-89% Biosorption Shamshad et al. (2016)
Chlorella vulgaris 64.76% Biosorption Wong et al. (2000)
Scenedesmus 61.2 % Biosorption Wang and Wood (1984)
Chlorella miniate 1367.62 μg/g Biosorption Wong et al. (2000)
V. debaryana 14.9 mg/g Biosorption Shamshad et al. (2020)

dichlorodiphenyltrichloroethane (DDT), can accumulate and cell organelles. Bioremediation techniques for nickel
in the whole cell system, leading to various bio-processes decontamination have included the use of probiotic micro-
such as interaction with organisms, surface sorption, trans- organisms (Beglari et al. 2022). The cell walls of plants
portation inside and outside the cell, intracellular precipi- and microbes are composed of carbohydrates, proteins, and
tation, or translocation inside vacuoles. Living organisms lipids, which contain functional groups on their surface
utilize pollutants as sources of nutrition and energy, cata- that facilitate the adsorption of contaminants like Ni(II).
lyzing them into less harmful forms. In some cases, micro- Combining the surface functional groups and accumulation
organisms export pollutants outside the cell through efflux mechanisms of metal-tolerant plants and microbes offers a
pumps to reduce their toxicity while maintaining cellular promising approach for nickel removal (Han et al. 2020;
homeostasis. Temperature, pH, moisture, initial metal con- Kumar and Dwivedi 2020; Priyadarshanee and Das 2021;
centration, chemical nature of the pollutant, availability of Kumar and Dwivedi 2021).
nutrients, and microbial community of the contaminated Wastewater treatment remains a significant challenge in
area are significant factors that can affect the bioremedia- the pursuit of sustainability (Fig. 5). Various biotechnology-
tion process (Kumar and Dwivedi 2021). Increasing the based wastewater treatment technologies are being devel-
pH to 4 has been shown to enhance the removal percentage oped, including activated sludge (AS), oxidation ponds,
of Ni(II) ions, while further increasing the pH causes the droplet filters, biofilters, and anaerobic treatments. Biotech-
percentage to decrease (Talaee Shoar et al. 2022). nology is also utilized in environmental engineering through
Metal-tolerant microorganisms and plants have the abil- processes such as bio-trickling filters, solid composting, and
ity to accumulate high levels of nickel in their cytoplasm biosorption. The key to successful treatment lies in finding

13
40230 Environmental Science and Pollution Research (2024) 31:40224–40244

Fig. 5  Schematic representation


of wastewater treatment process

the appropriate microbes capable of degrading heavy met- Researchers, such as Colussi et al. (2010), have explored
als and implementing the treatment measures in the right the utilization of anaerobic sludge for nickel sorption and
conditions. Therefore, review papers focusing on the det- investigated the impact of nickel removal on methane gen-
rimental effects of nickel on the environment, plants, and eration. Their study demonstrated the potential of anaerobic
human health, as well as the physicochemical techniques sludge in sorbing nickel while shedding light on the rela-
for heavy metal removal and the mechanisms of heavy metal tionship between nickel removal and methane production.
removal using microorganisms, are crucial for advancing our Additionally, Niec and Cha (2000) conducted research on
understanding of this field. the biosorption of Ni(II) using industrial anaerobic sludge in
a batch reactor. They discovered the effectiveness of anaero-
Activated sludge bic sludge in removing nickel under specific conditions of
temperature and pH. Niec and Cha further investigated the
Activated sludge (AS) and membrane bioreactors are highly effect of anoxic selectors on heavy metal removal by acti-
promising wastewater treatment technologies. Activated vated sludge. By comparing the metal binding properties of
sludge systems provide a cost-effective means of remov- activated sludge systems with and without anoxic selectors,
ing contaminants through physical and chemical adsorption they found that the selection sludge exhibited significantly
processes. Activated sludge is a widely adopted and cost- higher sorption capacity compared to the control sludge.
effective wastewater treatment technology that plays a cru- These studies highlight the potential of activated sludge sys-
cial role in mitigating water pollution. Activated sludge flocs tems in efficiently removing heavy metals and emphasize the
are predominantly composed of hydrophilic polar materials, importance of optimizing process parameters for enhanced
and these flocs contain a substantial amount of contaminants contaminant removal.
(Buaisha et al. 2020). When wastewater comes into contact
with activated sludge flocs, various pollutants, including Membrane bioreactor
heavy metals, natural contaminants, and air pollutants, can
be effectively targeted for removal. This removal is accom- Membrane bioreactors (MBR) integrate biological pro-
plished through a range of physical and chemical adsorption cesses with membrane separation, offering advantages such
processes. as modularity, ease of measurement, and compatibility with
Gravity settling, ion exchange, bonding, non-polar pre- various applications. Advancements in both activated sludge
cipitation, oxide depletion, enzymatic reactions, and elec- and membrane bioreactor technologies hold significant
trical adsorption are some of the mechanisms involved in potential for improving wastewater treatment efficiency and
the physical and chemical adsorption processes associated addressing the challenges associated with water pollution.
with activated sludge treatment (Buaisha et al. 2020). These The MBR represents a class of water and wastewa-
mechanisms enable the efficient capture and removal of con- ter treatment systems that combine biological processes
taminants from wastewater, enhancing the overall treatment with membrane separation techniques (Fig. 6). Membrane
performance. technology has gained significant attention in wastewater

13
Environmental Science and Pollution Research (2024) 31:40224–40244 40231

During the RBC process, the wastewater flows over the


rotating discs, allowing the microorganisms in the biofilm to
come into contact with the pollutants present in the waste-
water. The microorganisms, including bacteria and other
microbes, degrade and assimilate the organic matter and
contaminants, thereby purifying the water.
One of the significant advantages of RBC is its ability
to remove priority pollutants, such as pharmaceuticals and
personal care products, from wastewater. Studies have shown
that the RBC process is effective in the removal of these
pollutants (Hassard et al. 2015). The high-density commu-
Fig. 6  Schematic illustration of membrane bioreactor
nication surface provided by the rotating discs facilitates
the interaction between the pollutants and microorganisms,
enhancing the efficiency of pollutant removal.
treatment due to its modular design, ease of measurement, After passing through the RBC, the treated wastewater
minimal footprint, and compatibility with other processes. is transported to a clarifier, where the suspended biological
The MBR has emerged as an attractive and innovative tech- particles settle as sludge. The sludge can then be further
nique to overcome challenges associated with conventional treated or disposed of properly. RBC offers several advan-
activated sludge processes, including low concentrations of tages, including low cost, simplicity, process durability, and
strong mixed alcohol, poor sludge settling, and biological eco-friendly performance. For example, research by Rana
instability (Darweesh et al. 2021). et al. (2018) demonstrated that the RBC process improved
MBRs have demonstrated their capacity to effectively the efficiency of phenol removal by more than 56%. This
treat wastewater from various sources, including industrial highlights the effectiveness of RBC in treating specific con-
and domestic sectors. Although certain existing water treat- taminants present in wastewater.
ment systems may currently outperform MBRs in terms of
cost and operational capabilities, projected advancements Bioleaching or biomining
in bioreactor design and waste removal efficiency hold the
promise of making the MBR system a viable option for effi- Bioleaching, also known as biomining, is a process that uti-
cient wastewater management in the near future (Khan et al. lizes microorganisms, such as bacteria or archaea, to extract
2018). valuable metals from low-grade ores. This technique is con-
Notably, submerged membrane bioreactor (SMBR) con- sidered more efficient and environmentally friendly com-
figurations have exhibited remarkable capabilities in the pared to traditional mining methods. Bioleaching can also
removal of antibiotics from contaminated sources, thereby be applied to the remediation of mine tailings and electronic
reducing the environmental risks associated with these waste. Figure 7 exhibits the schematic illustration of the pro-
pharmaceutical compounds (Xu et al. 2019). Furthermore, cess of bioleaching.
SMBRs have been shown to remove up to 60% of organic The bioleaching process can be carried out through dif-
and nutrient-rich waste, underscoring their potential in sus- ferent methods, including slope leaching, heap leaching,
tainable wastewater treatment practices. These findings sug- and in situ leaching. In slope leaching, the ore is stacked
gest that membrane bioreactors, with their ability to com- on a slope and irrigated with a leaching solution, allowing
bine biological and membrane separation processes, offer the microorganisms to interact with the ore and extract the
a promising approach for the effective treatment of diverse metals. Heap leaching involves piling the ore in a heap and
wastewater streams. percolating it with a leaching solution. In in situ leaching,
the leaching solution is injected directly into the ore deposit.
Rotating biological contractor Bioleaching is effective even at ambient temperatures below
30 °C, making it suitable for various environments (Riek-
The rotating biological contactor (RBC) is a secondary treat- kola-Vanhanen 2013). The microorganisms involved in
ment technique used in wastewater treatment plants after the bioleaching oxidize the sulfide minerals present in the ore,
primary treatment process. The primary treatment involves releasing metal ions that can be solubilized and recovered.
the removal of large solids through screening and settling Different metals, including nickel, zinc, cobalt, gold, ura-
of suspended solids. The RBC process utilizes a series of nium, silver, and copper, can be extracted through bioleach-
rotating discs or drums that are partially submerged in the ing. The efficiency of metal extraction depends on various
wastewater. These discs are coated with a biological film, factors, such as the ore composition, microbial activity, pH,
which serves as a medium for microbial growth. and temperature. For instance, a study by Cameron et al.

13
40232 Environmental Science and Pollution Research (2024) 31:40224–40244

Fig. 7  Schematic illustration for


the process of bioleaching

(2009) investigated the technical viability of elevated-pH particularly bacteria, through active metabolic processes.
bioleaching on a low-grade ultramafic nickel sulfide ore. The Bacterial cells employ proteins, such as transporters, to
research demonstrated that nickel extraction from pentland- take up heavy metals from their surroundings and seques-
ite was relatively insensitive to acidity at low pH but sensi- ter them within the cell (Fig. 8). Bioaccumulation occurs
tive at high pH. The study achieved significant recovery of when the absorption rate of contaminants exceeds the rate
nickel, cobalt, and copper through flask and column leaching of loss. The initial phase is assumed to be the adsorption
processes. of Heavy metals (HMs) onto the cells, and the metal spe-
cies are then carried into the cells, where the HMs can
Bioaccumulation be sequestered by proteins, the lipid bilayer as an import
system, and peptide ligands as a storage system through
Bioaccumulation refers to the process by which substances, the cell metabolic cycle (Mishra and Malik 2013).
such as pesticides or toxins, accumulate in an organism The process of bioaccumulation is influenced by the
over time. Chemicals can enter an organism through vari- rate of absorption of contaminants compared to their
ous routes, including inhalation, skin absorption, or inges- elimination rate. Bacterial cells adsorb heavy metals onto
tion. Bioconcentration occurs when the concentration of a their surfaces, and the metals are subsequently transported
chemical within an organism exceeds that of its surrounding into the cells. Inside the cells, proteins, lipid bilayers, and
environment, such as air or water. Biomagnification, on the peptide ligands can sequester the heavy metals, leading to
other hand, refers to the increase in chemical concentration their accumulation (Mishra and Malik 2013).
as it moves up the food chain. As a result, this mechanism is reliant on the metabolism
In other words, the steady accumulation of substances of bacterial cells. According to research by Xujia Wu pub-
in an organism, such as pesticides or other toxins, is known lished in 2021, the ability of a marine Brevibacterium sp.
as bioaccumulation (Alexander 1999). Chemicals can be known as X6 to accumulate nickel was examined in order
absorbed by an organism through breathing, skin absorption, to determine whether it might be used to bioremediate
or ingestion. Bioconcentration occurs when the concentra- ­Ni2+ contaminants in marine settings. The maximal ­Ni2+
tion of a chemical within an organism exceeds that of its bioaccumulation and minimum N ­ i2+ inhibitory concen-
surroundings (air or water). Bioaccumulation of chemicals tration of X6 were greater than those of most reported
in the body due to direct detection from the natural matrix strains, at 1000 mg/L and 100.95 mg/g, respectively. A
(bioconcentration) and acquisition from food, according bioaccumulation test conducted in different research by
to the International Union of Pure and Applied Chemistry Beglari et al. (2022) yielded an approximate rate of nickel
(biomagnification). accumulation inside the strains’ cells. The best nickel
In the case of heavy metals, bioaccumulation involves accumulation rate was recorded by L. casei, L. brevis, and
the uptake and accumulation of these metals by organisms, L. mocusae at around 43%, followed by B. infantis.

13
Environmental Science and Pollution Research (2024) 31:40224–40244 40233

Fig. 8  Schematic illustration for the bioaccumulation of heavy metals through the food chain

Biotransformation microbial growth rate and a specific quick rate of degenera-


tion. Environmental biotransformation approaches, on the
Biotransformation refers to the biological conversion of one other hand, have issues.
chemical compound or a mixture of compounds into differ-
ent forms. Microorganisms, including fungi and bacteria, are Plant growth‑promoting bacteria
capable of carrying out biotransformation processes. These
microorganisms can use whole cells, cell lysates, or purified Plant growth-promoting bacteria (PGPB) are a group of
enzymes to catalyze the transformation reactions. beneficial microbes associated with plants that play impor-
Biotransformation plays a crucial role in the breakdown tant roles in promoting plant growth, development, and
and elimination of hazardous contaminants in water bodies, stress resistance (Middleton et al. 2021). These bacteria
contributing to their remediation. Microorganisms utilize have been particularly studied in the context of Ni hyperac-
various metabolic pathways and enzymes to transform toxic cumulator species, which are plants capable of accumulat-
compounds into less harmful and more stable forms. Natural ing high levels of nickel. PGPB enhance the growth and
biotransformation relies on the activity of indigenous micro- development of plants, including Ni hyperaccumulators,
organisms to degrade and eliminate contaminants in water by various mechanisms (Fig. 4). They can produce com-
bodies, restoring them to their original state. The growth pounds that stimulate plant growth, such as indole-3-acetic
of microorganisms is facilitated by favorable environmen- acid (IAA), which is a phytohormone involved in root and
tal conditions, and their metabolic processes contribute to shoot development. PGPB can also produce enzymes, such
the degradation of pollutants. Environmental biotransfor- as 1-aminocyclopropane-1-carboxylic acid (ACC) deami-
mation approaches can be employed to enhance the natural nase, which helps plants cope with high ethylene concen-
biotransformation process. However, these approaches face trations that can hinder root growth. Studies have shown
challenges due to the complex nature of pollutants and the that inoculation with specific PGPB strains can increase the
need for optimal microbial growth conditions. levels of ACC deaminase and IAA in Ni hyperaccumulator
Biotransformation is the process of microorganisms such plants, leading to improved growth and Ni phytoextrac-
as fungi, bacteria, and their enzymes converting hazardous tion in polluted soil. For example, Babu et al. (2013) and
contaminants into less dangerous and lasting forms (Alva- Kamran et al. (2016) demonstrated the positive effects of
rino et al. 2018). Natural biotransformation is a process that PGPB inoculation on Ni hyperaccumulators. Specific bac-
uses normal microorganisms to break down and eliminate terial strains, such as Arthrobacter nicotinovorans SA40
toxins in water bodies, restoring them to their original state and Bacillus subtilis strain SJ-101, have been found to be
(Alvarino et al. 2018). Microorganisms must convert water effective in extracting Ni and reducing Ni phytotoxicity,
pollution into harmless product forms tobio transform, while respectively. The effectiveness of PGPB inoculation for
natural conditions facilitate and simplify microbial growth. increased Ni bioremediation needs to be further investi-
Natural characteristics should be included to obtain a low gated through field applications.

13
40234 Environmental Science and Pollution Research (2024) 31:40224–40244

Through increased growth and development (length, dry contamination of the surrounding environment. Phytovola-
biomass of root and shoot, root girth, total chlorophyll, and tilization is a process in which plants absorb pollutants,
N contents of shoots) of heavy metals in hyperaccumula- such as volatile organic compounds (VOCs), and release
tor species including Ni, PGPBs improve metal tolerance them into the atmosphere through transpiration. However,
and supports (Ma et al. 2011; Basu et al. 2017). The three phytovolatilization is not effective for Ni cleanup. In the
different inoculants were found to increase 1-aminocyclo- case of phytoextraction, plants take up pollutants from
propane-1-carboxylic acid deaminase (ACC deaminase) and the soil and accumulate them in their shoots or leaves.
indole-3-acetic acid (IAA) levels in Ni hyperaccumulators This process is particularly relevant for heavy metals like
and to improve Ni phytoextraction in polluted soil (Babu nickel. Certain plant species, such as Pycnandra acumi-
et al. 2013; Kamran et al. 2016). Plant roots are hampered nata (formerly Sebertia acuminata) found in New Caledo-
by high ethylene concentrations; however, ACC deaminase nia, have the remarkable ability to accumulate high levels
can hydrolyze ethylene and stimulate the formation of plant of nickel in their tissues.
biomass for Ni Bioremediation (Cabello-Conejo et al. 2014), Phytoremediation offers a sustainable and environmen-
reported Arthrobacter nicotinovorans SA40 was shown to be tally friendly approach to remediate contaminated sites.
particularly successful at extracting Ni from contaminated However, the effectiveness of phytoremediation depends
soil. Bacillus subtilis strain SJ-101, according to (Zaidi et al. on various factors, including plant species selection, pol-
2006), reduces Ni phytotoxicity. Plant growth-promoting lutant characteristics, and site conditions. Further research
bacteria (PGPBs) increased Ni uptake in Alyssum murale, is needed to optimize phytoremediation strategies and
according to (Abou Shanab et al. 2003). Individual PGPBs explore the potential of different plant species for specific
and consortia must be tested for their efficacy in field appli- contaminants
cations for increased Ni bioremediation. Phytostabilization stabilizes Ni in the vadose zone
of plants by accumulating/precipitating into the plants’
Phytoremediation belowground parts/zone (Bolan et al. 2011), reducing
further Ni pollution in the area (Fig. 9). Heavy metals,
Phytoremediation is a remediation technique that utilizes particularly mercury (Hg), are assimilated into volatile
plants to remove, degrade, or immobilize pollutants, par- organic compounds (VOCs) by plants and released into
ticularly heavy metals, from contaminated soil, water, or the atmosphere by transpiration (Marques et al. 2009). The
air. Phytoremediation can be divided into different pro- phytovolatilization process is ineffective for Ni clean-up.
cesses, including phytostabilization, phytovolatilization, According to Jaffrè et al. (2018), a unique tree in New
and phytoextraction. Phytostabilization involves the use Caledonia called Pycnandra acuminata (formerly Sebertia
of plants to immobilize or stabilize pollutants in the soil, acuminata) has a remarkable capacity to collect nickel in
preventing their movement or leaching. Plants accumulate its blue-green latek since nickel makes up around 25% of
the pollutants in their belowground parts, reducing further the dry weight of the latek.

Fig. 9  Schematic illustration for


the phytoremediation of heavy
metals

13
Environmental Science and Pollution Research (2024) 31:40224–40244 40235

Role of microorganisms in the removal In addition to their organic pollutant degradation capabili-
of heavy metals ties, fungi also play a role in heavy metal removal (Taran et al.
2015; Sundararaju et al. 2020; Sharma et al. 2022). Various
Microorganisms, including bacteria, fungi, and algae, play processes such as heavy metal accumulation, detoxification,
important roles in the removal of heavy metals from various mineralization, and transformation have been reported in
environments. These microorganisms utilize different mech- fungi (Table 2). For instance, Phanerochaete chrysosporium
anisms such as bio-precipitation, biosorption, and intracellu- has been studied for its ability to remove Ni through a process
lar accumulation to sequester and detoxify heavy metal ions. called biosorption. Under well-mixed conditions, P. chrys-
Harnessing the abilities of microorganisms for bioremedia- osporium can accumulate up to 16 mg/L of Ni with a high
tion purposes offers promising solutions for mitigating heavy clearance efficiency (Noormohamadi et al. 2019).
metal pollution and restoring contaminated ecosystems. The diverse enzymatic and metabolic activities of fungi
make them promising candidates for bioremediation approaches
aimed at heavy metal removal and environmental cleanup.
Bacteria Table 2 provides a list of different fungi that have been stud-
ied for their involvement in Ni removal. These fungi serve as
Microorganisms, particularly bacteria, play a significant role promising candidates for bioremediation strategies targeting
in the removal of heavy metals from various environments. the removal of heavy metals from contaminated environments.
Both Gram-negative and Gram-positive bacteria have dem-
onstrated high efficacy in removing heavy metals such as
nickel (Ni). For example, Bacillus aryabhattai HU-39 has Algae
been shown to effectively remove Ni(II). In a study, strain
HU-39 achieved a removal efficiency of 89% at an initial Algae, with their unique biological characteristics, also
Ni(II) concentration of 250 mg/L and a temperature of 30 play a significant role in the removal of heavy metals.
°C. The removal of Ni(II) occurs through a process called Algae exhibit high photosynthetic competency and possess
bio-precipitation, where Ni(II) is converted into ­NiCO3, a a simple structure, allowing them to thrive in challenging
precipitated form of nickel (Khadim et al. 2019). ecological settings such as environments with high salin-
Other bacteria such as Bacillus megaterium 1295S and ity, heavy metal contamination, nutrient stress, and high
Sporosarcina pasteurii 586S have also been investigated for temperatures (Leong and Chang 2020).
their ability to remove Ni (Gheethi et al. 2017). The mecha- In addition to their environmental adaptability, algae have
nisms involved in Ni(II) elimination by these bacteria include the ability to accumulate heavy metals and produce biomass.
intracellular accumulation and surface sorption, both driven This dual strategy makes them useful for wastewater treat-
by the presence of functional groups on the bacterial cell sur- ment and energy production. Algae have been utilized for the
face (Khadim et al. 2019). These functional groups interact removal of heavy metals such as chromium (Cr) and nickel
with Ni(II) ions, facilitating their removal from the environ- (Ni) in both live and dead forms (Table 3). The mechanisms
ment (Yang et al. 2011; Wierzba 2017; Wu et al. 2021). involved in heavy metal removal by algae include biosorp-
Table 1 provides a list of different bacteria that have tion, where the heavy metal ions are adsorbed onto the sur-
been studied for their involvement in Ni removal. These face of algae, as well as intracellular uptake and accumula-
bacteria serve as promising candidates for bioremediation tion (Ramadoss and Subramaniam 2019).
strategies targeting the removal of heavy metals from con- Algae-based bioremediation approaches have gained atten-
taminated environments. tion due to their eco-friendly nature and potential for sustain-
able applications in heavy metal removal from contaminated
waters and wastewaters. Table 3 provides a list of different
Fungi algae that have been served as promising candidates for biore-
mediation strategies targeting the removal of heavy metals
Fungi are essential components of ecosystems and pos- from contaminated environments (Shamshad et al. 2020).
sess saprophytic qualities, allowing them to contribute to
the organic cleansing of the environment. They have been
extensively studied for their potential in degrading organic Mechanisms involved in heavy metal
pollutants and are used in various industries, including food biosorption
and beverage production. Fungi possess a wide range of
enzymes that can be harnessed for environmental remedia- The biosorption mechanism is a complex process that uti-
tion purposes (Singh et al. 2019; Singh and Dwivedi 2020). lizes bio-sorbents for binding sorbates into it. Many natural
resources such as microbial biomass (bacterial, fungal, algal

13
40236 Environmental Science and Pollution Research (2024) 31:40224–40244

biomass), agricultural waste, industrial by-products, etc. are present on the bacterial cell surfaces contribute to Cd bind-
used as bio-sorbents. Biosorption can remove pollutants even ing by complex formation (Machalová et al. 2015). In the ion
in a significantly lower concentration and take out heavy met- exchange mechanism, the exchange of binary metal cations
als present in even ppb (parts per billion) concentration from occurs with the counter ion residing on the surface of the
a polluted environment (Ahemad and Kibret 2013). Several biosorbent. An ion exchange process was identified for Pb(II)
ways are adapted by the bacteria to take up these metals and adsorption by extracellular polymeric substances (EPS) of
classified according to various criteria. Depending on cell Klebsiella sp. J1 with the counter ions ­K+ and ­Mg2+ (Wei
metabolism, biosorption is categorized into metabolism- et al. 2016). The mechanism of metal binding by precipita-
dependent and metabolism-independent. According to the tion occurs through the reaction of metal ions with the func-
metal absorption/accumulation location, biosorption can be tional groups present on the bacterial surface which results
classified as extracellular precipitation, cell surface sorption, in insoluble organic metal precipitates and remains attached
and intracellular accumulation (Fig. 10). In metabolism- to the microbial cells. Removal of some of the toxic heavy
dependent biosorption, intracellular accumulation of metals metals such as Ni(II), Cd(II), Cr(III), Cr(VI), and Co(II) from
occurs through the cell membrane, carried out by viable cells various industrial effluent was carried out by Escherichia coli
only. Metal uptake in metabolism-independent biosorption C90, that produces alkaline phosphatase to precipitate the
occurs by physicochemical interaction between the functional metal cations (Chaudhuri et al. 2013). Physical adsorption of
groups on the surface of bacteria and the metal ions. The metals on the microbial surface takes place by van der Waals
binding of metal ions onto the cell surface of a bacterium in forces between the biomass and metal ions. Biosorption of
metabolism-independent biosorption involves various mecha- Cd and Cr ions from metal solutions was effectively done
nisms such as physical interaction (electrostatic or van der by applying Bacillus laterosporus and Bacillus licheniformis
Waals interaction) or chemical interaction (displacement of (Zouboulis et al. 2004). The transport of heavy metals across
attached metal cations by ion exchange), complexation, dif- the cell membrane by living bacteria occurs in two steps.
fusion, surface adsorption, or by precipitation. Complexa- The first step is independent of metabolism, which involves
tion involves associating two or more species, i.e., metal ions the attachment of heavy metals to the cell surface. The sec-
and the functional groups present on the bacterial cell sur- ond one is the internalization of metal ions across the cell
face. It is categorized into two different types: monodentate membrane (Das et al. 2008b). This mechanism is similar to
and polydentate complex (Kanamarlapudi et al. 2018). In the uptake of some essential ions such as N ­ a+, ­K+, ­Ca2+,
monodentate complexes, the metal ion binds with the ligands etc. by the cells. Thus, the ion channels may be confused by
via covalent bonds. It occupies the ligand's central position, the metal cations having identical charges and ionic radius
but in polydentate complexes, more than one metal ion inter- associated with essential ions.
acts with the ligands. The Fourier-transformed infrared spec- Cells employ various defense mechanisms against high
troscopy (FTIR) analysis of the non-living biomass of Kocu- concentrations of nickel, including nickel efflux. Interest-
ria palustris and Micrococcus luteus showed that carboxylate ingly, cells also exhibit chemotactic responses to nickel
ions and functional groups such as amino and phosphate concentrations in the environment. Englert et al. (2010)

Fig. 10  Schematic illustration


for the mechanism of biosorp-
tion

13
Environmental Science and Pollution Research (2024) 31:40224–40244 40237

demonstrated that nickel has a chemotactic-repellent effect Pseudomonas aeruginosa strains accumulate nickel within
mediated by the methyl-accepting chemotaxis protein Tar, their cells, and energy-dispersive X-ray analysis reveals the
independent of NikA. presence of metallic nickel (Sar et al. 2001). Moreover, Thio-
Saccharomyces cerevisiae strains known for their nickel capsa roseopersicina, when grown on hydrogen gas, exhibits
resistance have long been recognized for their ability to reduction of Ni(II) to elemental nickel, which is associated
sequester the metal in vacuolar compartments along with with increased nickel resistance.
high levels of the amino acid histidine (Joho et al. 1992). Several factors influence the biosorption mechanisms
Studies have shown that strains with defective vacuolar involved in the removal of heavy metals, including nickel.
proton ATPase, impairing vacuolar acidification, display These factors include (i) the properties of the biosorbents,
increased nickel toxicity. Genetic investigations have whether living or non-living; (ii) the characteristics of the
revealed that histidine auxotrophs exhibit heightened sen- targeted metal; (iii) the type of binding sites involved in
sitivity not only to nickel but also to various other metals. metal sequestration (biological ligands); (iv) various param-
Furthermore, knockout mutants of genetic iron importers eters of the biosorption process, such as temperature, pH,
in yeast cells have shown increased sensitivity to nickel contact time, and the amount of sorbent and sorbate; and (v)
(Ruotolo et al. 2008). Genome-wide studies in S. cerevisiae the characteristics of the metal solution, including the pres-
have identified 149 genes whose deletion enhances nickel ence of competing co-ions. Consideration of these factors is
sensitivity, indicating their involvement in nickel resistance crucial in designing efficient biosorption strategies for the
(Arita et al. 2009). These genes include cation transport- removal of heavy metals from contaminated environments.
ers, siderophore-iron transporters, diphthamide production
genes, and proton-transporting ATPase-related genes.
Sulfate-reducing bacteria are capable of producing sig-
nificant amounts of sulfide, which can mitigate the toxicity Merits and demerits of Ni removal approach
of metals. For example, a nickel-resistant strain of desulfo-
tomaculum grown in the presence of high nickel concentra- The removal of nickel (Ni) from contaminated environments
tions generates a dark-brown, soluble nickel-sulfide product, involves various remediation approaches, each with its own
effectively reducing the concentration of free nickel ions merits and limitations. In order to better understand the effec-
(Fortin et al. 1994). In the case of Pseudomonas putida S4, tiveness and feasibility of these approaches, several studies
nickel accumulation occurs in the periplasm, potentially (Gong et al. 2018; Yadav et al. 2018) have provided insights
facilitated by an 18 kDa protein, as a resistance mechanism into the advantages and disadvantages associated with differ-
against nickel (Tripathi and Srivastava 2006). In contrast, ent techniques for Ni removal. Table 4 summarizes the various

Table 4  Comparison of techniques for heavy metal removal, including nickel and their pros and cons
Techniques used for removal Advantages Disadvantages

Replacement of soil • Suitable for the remediation of deeply contaminated • Costly


soil • Loss of fertility from the soil occurs
Electro remediation • Suitable for quick remediation • Not effective for the soil contaminated from the depth
• Require low energy • Reduces the effectiveness of the soil
Immobilization techniques • Cost-effective • No complete removal
• Easy to use
• Rapid technique
Washing of soil • Effective for highly contaminated sites • Change in properties of the soil
• Quick method • Costly technique
• Downturn in the soil structure
Bioremediation • Cost-effective • Time-consuming technique
• Minimal site disruption • Highly specific
Environmental-friendly • Sensitive to toxins as it releases toxic metabolites
• High efficiency for metal removal
• Very effective for field application with high confi-
dence
• Removes contaminated wastes permanently.
• Highly public acceptance
Phytoextraction • Produce low waste • Time-consuming
• Cost-effective technique • Biomass of plant needs to be disposed

13
40238 Environmental Science and Pollution Research (2024) 31:40224–40244

techniques used for the removal of heavy metals, including crucial in addressing this issue. Additionally, investigating
nickel, along with their respective merits and limitations. It ways to mitigate oxidative stress caused by nickel toxicity
serves as a comprehensive reference for evaluating the effi- is necessary.
cacy and practicality of each approach. Bioremediation offers a promising solution for the
The advantages of specific Ni removal techniques can removal of toxic heavy metals from contaminated water.
include high efficiency in metal sequestration, cost-effective- Efforts should be focused on decontaminating Ni at differ-
ness, eco-friendliness, and compatibility with different environ- ent trophic levels using various remediation technologies,
mental conditions. For example, certain methods may exhibit including transgenic phytoremediation and phytoextraction.
a high removal efficiency for Ni ions, effectively reducing their It is important to elucidate the interactions between micro-
concentration to acceptable levels. Other techniques may prove bial consortia and microorganisms involved in Ni phytore-
to be economically viable, requiring less investment or utiliz- mediation by screening potential plant species and microbes.
ing readily available materials. Additionally, some approaches Understanding the functions, activities, and regulation of
may be environmentally sustainable, ensuring minimal negative enzymes involved in Ni bioremediation, as well as devel-
impact on the ecosystem. Furthermore, certain methods may oping high-throughput Ni removal techniques, is essential.
be adaptable to different environmental settings, making them Furthermore, in-depth investigations are required to
applicable in a wide range of scenarios. comprehend the biological mechanisms of Ni toxicity in
However, it is important to consider the limitations and prokaryotes. It is necessary to conduct immediate research
drawbacks associated with each Ni removal approach. Some on Ni toxicity and essentiality in changing environmental
techniques may have lower removal efficiencies or may be circumstances, such as climate change, to assess the long-
ineffective in treating certain forms of Ni contamination. term effectiveness of bioremediation treatments in the
Cost considerations, such as the need for expensive equip- field. Identifying, controlling, and transferring beneficial
ment or specialized materials, can limit the feasibility of cer- traits involved in Ni bioremediation, as well as enhancing
tain methods, particularly in resource-constrained settings. the performance of existing species, will aid in reducing
Moreover, some approaches may produce by-products or pollution in the food chain. Establishing regulations and
generate secondary waste streams, potentially posing addi- laws that promote the use of Ni accumulator species as
tional environmental concerns. The compatibility of a tech- effective bioremediation techniques is also crucial.
nique with specific environmental conditions, such as pH or In summary, addressing the challenges associated with
temperature, may also restrict its applicability. nickel contamination requires multidisciplinary research
By evaluating the advantages and disadvantages of differ- efforts, including molecular studies, bioremediation strat-
ent Ni removal techniques, researchers, policymakers, and egies, and regulatory frameworks. By focusing on these
environmental practitioners can make informed decisions aspects, we can develop sustainable approaches to miti-
regarding the most suitable approach for a given situation. gate the environmental and health risks posed by excessive
It is essential to weigh the benefits and limitations carefully nickel levels and ensure the integrity of our ecosystems
in order to select an effective and sustainable method for the and food chains.
remediation of nickel-contaminated environments.
Acknowledgements The authors are grateful to all research staff that
contributed to the data collection required for this review article.

Conclusions and future prospective Author contributions Sonu Sharma, Monu Sharma, Raman Kumar, M.
Sayeed Akhtar, Ahmad Umar, Abdulrab Ahmed M. Alkhanjaf: inves-
tigation, methodology, validation, formal analysis, writing—original
In conclusion, nickel (Ni) is a versatile and essential metal, draft, and visualization. Ahmad Umar, Sotirios Baskoutas: writing—
but its presence in high concentrations poses significant envi- review and editing and data curation. All authors commented on the
ronmental hazards. It plays a crucial role as a micronutrient manuscript. All authors read and approved the final manuscript.
for plant growth, but variations in its concentration can dis-
Funding The Deanship of Scientific Research at Najran University,
rupt the entire plant cycle. Nickel has the potential to impact Najran, Kingdom of Saudi Arabia provided funding under the Research
vital environmental components such as soil and water due Group funding program grant no. NU/RG/MRC/12/2.
to its transition activity. While it is necessary for bacterial
processes, excessive nickel can lead to toxicity by interfering Data availability All data collected and reviewed are included in this
article and properly referenced.
with enzyme activity and physiological processes, as well as
causing deficiencies in other essential nutrients.
Declarations
To ensure sustainable food production systems, fur-
ther research is needed, particularly in understanding the Ethics approval We certify that the manuscript titled “Bacterial-
molecular mechanisms of nickel transport and accumulation. assisted bio remedial removal of nickel ions: A Review” (hereinafter
referred to as “the Paper”) is entirely our original work, and it does
Developing Ni tolerance and homeostasis mechanisms is

13
Environmental Science and Pollution Research (2024) 31:40224–40244 40239

not infringe the copyright of any third party. The submission of the Arita A, Zhou X, Ellen TP, Liu X, Bai J, Rooney JP, Kurtz A, Klein
Paper to Environmental Science and Pollution Research implies that CB, Dai W, Begley TJ, Costa M (2009) A genome-wide dele-
the paper has not been published previously. This work is not under tion mutant screen identifies pathways affected by nickel sul-
consideration for publication elsewhere. Its publication is approved fate in Saccharomyces cerevisiae. BMC Genomics 10:524.
by all authors and, if accepted, it will not be published elsewhere in https://​doi.​org/​10.​1186/​1471-​2164-​10-​524
the same form, either in English or in any other language, without Azimi A, Azari A, Rezakazemi M, Ansarpour M (2017) Removal of
the written consent of the Publisher. Copyrights for articles published heavy metals from industrial wastewaters: a review. ChemBio-
in Environmental Science and Pollution Research are retained by the Eng Rev 4(1):37–59. https://​doi.​org/​10.​1002/​cben.​20160​0010
authors, with first publication rights granted to Environmental Science Babu AG, Kim JD, Oh BT (2013) Enhancement of heavy metal phy-
and Pollution Research. toremediation by Alnus firma with endophytic Bacillus thur-
ingiensis GDB-1. J Hazard Mater 250:477–483. https://​doi.​org/​
Consent to participate We affirm that all authors have participated in 10.​1016/j.​jhazm​at.​2013.​02.​014
the research work and are fully aware of ethical responsibilities. Bai M, Lu Y, Zhang Z, Cao K, Cai L, Li H (2022) Relationship
between microscopic pore structure and strength of cement-
Consent for publication We affirm that all authors have agreed for sub- based materials with low water-binder ratio under sulfate
mission of the Paper to ESPR and are fully aware of ethical respon- attack environment. Sci Adv Mater 14(4):725–735. https://​
sibilities. doi.​org/​10.​1166/​sam.​2022.​4254
Barrera-Díaz CE, Lugo-Lugo V, Bilyeu B (2012) A review of chemi-
Competing interests The authors declare no competing interests. cal, electrochemical and biological methods for aqueous Cr
(VI) reduction. J Hazard Mater 223:1–12. https://​doi.​org/​10.​
1016/j.​jhazm​at.​2012.​04.​054
Basu S, Rabara R, Negi S (2017) Towards a better greener future-
an alternative strategy using biofertilizers. I: Plant growth
promoting bacteria. Plant Gene 12:43–49. https://​doi.​org/​10.​
References 1016/j.​plgene.​2017.​07.​004
Bawazeer TM (2022) Investigating the photocatalytic degradation of
Abdullah MM, Baker JH, Albargi HB, Jagnandan A, Ahmad MZ, N-chloropiperidine in aqueous solution by utilizing ­TiO2 under
Jebahi S, Algethami JS (2023) Environmental remediation blacklight illumination. Sci Adv Mater 14(4):772–778. https://​
via solution combustion route synthesis of single-phase ferro- doi.​org/​10.​1166/​sam.​2022.​4256
magnetic nickel doped zinc oxide (Ni-ZnO) nanostructure for Beglari S, Khodagholi F, Gholami Pourbadie H, Iranbakhsh A,
enhanced photocatalytic activity. Sci Adv Mater 15(2):169–175. Rohani M (2022) Biosorption and bioaccumulation of nickel
https://​doi.​org/​10.​1166/​sam.​2023.​4437 by probiotic lactic acid bacteria isolated from human feces.
Abou Shanab RA, Angle JS, Delorme TA, Chaney RL, Van Berkum P, Biorem J:1–12. https://​doi.​org/​10.​1080/​10889​868.​2022.​20865​
Moawad H, Ghozlan HA (2003) Rhizobacterial effects on nickel 29
extraction from soil and uptake by Alyssum murale. New Phy- Bishnoi NR, Sheoran IS, Singh R (1993) Effect of cadmium and nickel
tol 158(1):219–224. https://​doi.​org/​10.​1046/j.​1469-​8137.​2003.​ on mobilisation of food reserves and activities of hydrolytic
00721.x enzymes in germinating pigeon pea seeds. Biol Plant 35(4):583–
Acosta I, Gonzalez JFC, Perez ASR, Martinez VM, Zarate MDGM, 589. https://​doi.​org/​10.​1007/​BF029​28036
Castillo NCP (2018) Biosorption of heavy metals by Candida Bolan NS, Park JH, Robinson B, Naidu R, Huh KY (2011) Phytosta-
albicans. Chapters. https://​doi.​org/​10.​5772/​intec​hopen.​72454 bilization: a green approach to contaminant containment. Adv
Ahemad M, Kibret M (2013) Recent trends in microbial biosorption of Agron 112:145–204. https://d​ oi.o​ rg/1​ 0.1​ 016/B​ 978-0-1​ 2-3​ 85538-​
heavy metals: a review. Biochem Mol Biol 1(1):19–26. https://​ 1.​00004-4
doi.​org/​10.​12966/​bmb.​06.​02.​2013 Borja D, Nguyen KA, Silva RA, Park JH, Gupta V, Han Y, Kim H
Ahmad MSA, Ashraf M (2011) Essential roles and hazardous effects of (2016) Experiences and future challenges of bioleaching research
nickel in plants. Rev Environ Contam Toxicol 125-167. https://​ in South Korea. Minerals 6(4):128. https://​doi.​org/​10.​3390/​
doi.​org/​10.​1007/​978-1-​4614-​0668-6_6 min60​40128
Akhtar MJ, Ullah S, Ahmad I, Rauf A, Nadeem SM, Khan MY, Bul- Buaisha M, Balku S, Özalp-Yaman S (2020) Heavy metal removal
gariu L (2018) Nickel phytoextraction through bacterial inocula- investigation in conventional activated sludge systems. Civil Eng
tion in Raphanus sativus. Chemosphere 190:234–242. https://d​ oi.​ J 6(3):470–477. https://​doi.​org/​10.​28991/​cej-​2020-​03091​484
org/​10.​1016/j.​chemo​sphere.​2017.​09.​136 Burakov AE, Galunin EV, Burakova IV, Kucherova AE, Agarwal S,
Aksu Z, Açıkel Ü, Kabasakal E, Tezer S (2002) Equilibrium modelling Tkachev AG, Gupta VK (2018) Adsorption of heavy metals on
of individual and simultaneous biosorption of chromium (VI) and conventional and nanostructured materials for wastewater treat-
nickel (II) onto dried activated sludge. Water Res 36(12):3063– ment purposes: a review. Ecotoxicol Environ Saf 148:702–712.
3073. https://​doi.​org/​10.​1016/​S0043-​1354(01)​00530-9 https://​doi.​org/​10.​1016/j.​ecoenv.​2017.​11.​034
Alexander M (1999) Biodegradation and bioremediation. Gulf Pro- Cabello-Conejo MI, Becerra-Castro C, Prieto-Fernández A, Monter-
fessional Publishing roso C, Saavedra-Ferro A, Mench M, Kidd PS (2014) Rhizo-
Aloulou W, Aloulou H, Khemakhem M, Duplay J, Daramola MO, bacterial inoculants can improve nickel phytoextraction by the
Amar RB (2020) Synthesis and characterization of clay-based hyperaccumulator Alyssum pintodasilvae. Plant Soil 379:35–50.
ultrafiltration membranes supported on natural zeolite for https://​doi.​org/​10.​1007/​s11104-​014-​2043-7
removal of heavy metals from wastewater. Environ Technol Cameron RA, Lastra R, Mortazavi S, Bedard PL, Morin L, Gould WD,
Innov 18:100794. https://​doi.​org/​10.​1016/j.​eti.​2020.​100794 Kennedy KJ (2009) Bioleaching of a low-grade ultramafic nickel
Alvarino T, Suarez S, Lema J, Omil F (2018) Understanding the sulphide ore in stirred-tank reactors at elevated pH. Hydrometal-
sorption and biotransformation of organic micropollutants in lurgy 97(3-4):213–220. https://d​ oi.o​ rg/1​ 0.1​ 016/j.h​ ydrom
​ et.2​ 009.​
innovative biological wastewater treatment technologies. Sci 03.​002
Total Environ 615:297–306. https://​doi.​org/​10.​1016/j.​scito​tenv.​ Cecchi G, Roccotiello E, Di Piazza S, Riggi A, Mariotti MG, Zotti
2017.​09.​278 M (2017) Assessment of Ni accumulation capability by fungi

13
40240 Environmental Science and Pollution Research (2024) 31:40224–40244

for a possible approach to remove metals from soils and waters. metal pollution magnitudes: Health risk assessment of affected
J Environ Sci Health B52(3):166–170. https://​doi.​org/​10.​1080/​ cattle and human population in some rural regions, Qena, Egypt.
03601​234.​2017.​12615​39 J Adv Vet Anim Res 7(2):345. https://​doi.​org/​10.​5455/​2Fjav​ar.​
Chaudhuri G, Dey P, Dalal D, Venu-Babu P, Thilagaraj WR (2013) A 2020.​g428
novel approach to precipitation of heavy metals from industrial Ding C, Cheng W, Wang X, Wu ZY, Sun Y, Chen C, Yu SH (2020)
effluents and single-ion solutions using bacterial alkaline phos- Corrigendum: Competitive sorption of Pb (II), Cu (II) and Ni
phatase. Water Air Soil Pollut224:1–11. https://​doi.​org/​10.​1007/​ (II) on carbonaceous nanofibers: a spectroscopic and modeling
s11270-​013-​1625-y approach. J Hazard Mater389:122118–122118. https://​doi.​org/​
Chen Y, Zhao W, Zhao H, Dang J, Jin R, Chen Q (2020) Efficient 10.​1016/j.​jhazm​at.​2020.​122118
removal of Pb (II), Cd (II), Cu (II) and Ni (II) from aqueous Dong W, Gu W, Zhan Q, Wang A, Zhou J (2022) Study on the property
solutions by tetrazole-bonded bagasse. Chem Phys 529:110550. and mechanism of low content cement-industrial waste residue
https://​doi.​org/​10.​1016/j.​chemp​hys.​2019.​110550 silt solidification. Sci Adv Mater 14(12):1881–1892. https://​doi.​
Colussi I, Cortesi A, Gallo V, Solinas D, Vitanza R (2010) Removal org/​10.​1166/​sam.​2022.​4388
of nickel by sorption on anaerobic sludge. Effects on methane Dönmez G, Aksu Z (2001) Bioaccumulation of copper (II) and nickel
production. Chem Eng Trans 20:297. https://​doi.​org/​10.​3303/​ (II) by the non-adapted and adapted growing Candida sp. Water
CET10​20050 Res 35(6):1425–1434. https://​doi.​org/​10.​1016/​S0043-​1354(00)​
Coman V, Robotin B, Ilea P (2013) Nickel recovery/removal from 00394-8
industrial wastes: a review. Resour Conserv Recycl 73:229–238. Efome JE, Rana D, Matsuura T, Lan CQ (2019) Effects of operating
https://​doi.​org/​10.​1016/j.​resco​nrec.​2013.​01.​019 parameters and coexisting ions on the efficiency of heavy metal
Costa JM, da Costa JGDR, de Almeida Neto AF (2022) Techniques ions removal by nano-fibrous metal-organic framework mem-
of nickel (II) removal from electroplating industry wastewater: brane filtration process. Sci Total Environ 674:355–362. https://​
overview and trends. J Water Process Eng 46:102593. https://d​ oi.​ doi.​org/​10.​1016/j.​scito​tenv.​2019.​04.​187
org/​10.​1016/j.​jwpe.​2022.​102593 El-Sheekh MM, El-Abd MA, El-Diwany AI, Ismail AMS, Omar TH
da Silva Oliveira A, Bocio A, Beltramini Trevilato TM, Magosso (2015) Poly-3-hydroxybutyrate (PHB) production by Bacillus
Takayanagui AM, Domingo JL, Segura-Muñoz SI (2007) Heavy flexus ME-77 using some industrial wastes. Rendiconti Lincei
metals in untreated/treated urban effluent and sludge from a 26:109–119. https://​doi.​org/​10.​1007/​s12210-​014-​0368-z
biological wastewater treatment plant. Environ Sci Pollut Res Enayatizamir N, Liu J, Wang L, Lin X, Fu P (2020) Coupling lac-
14:483–489. https://​doi.​org/​10.​1065/​espr2​006.​10.​355 case production from Trametes pubescence with heavy metal
Dahmen-Ben Moussa I, Athmouni K, Chtourou H, Ayadi H, Sayadi S, removal for economic waste water treatment. J Water Process
Dhouib A (2018) Phycoremediation potential, physiological, and Eng 37:101357. https://​doi.​org/​10.​1016/j.​jwpe.​2020.​101357
biochemical response of Amphora subtropica and Dunaliella sp. Englert DL, Adase CA, Jayaraman A, Manson MD (2010) Repellent
to nickel pollution. J ApplPhycol 30:931–941. https://d​ oi.o​ rg/1​ 0.​ Taxis in Response to Nickel Ion Requires neither ­Ni2+ Transport
1007/​s10811-​017-​1315-z nor the Periplasmic NikA Binding Protein. J Bacteriol 192:2633–
Darweesh M, Zedan AM, El-Banna A, Elbasiuny H, Elbehiry F (2021) 2637. https://​doi.​org/​10.​1128/​jb.​00854-​09
Biotechnology for green future of wastewater treatment. https://​ Engwa GA, Ferdinand PU, Nwalo FN, Unachukwu MN (2019) Mecha-
doi.​org/​10.​1007/​698_​2021_​788 nism and health effects of heavy metal toxicity in humans. In:
Das N, Vimala R, Karthika P (2008a) Biosorption of heavy metals–an Poisoning in the modern world-new tricks for an old dog, vol 10,
overview. Ind J Biotechnol 7:159–169. http://​nopr.​niscpr.​res.​in/​ pp 70–90. https://​doi.​org/​10.​5772/​intec​hopen.​82511
handle/​12345​6789/​1822 Fortin D, Southam G, Beveridge TJ (1994) Nickel sulfide, iron-nickel
Das P, Mukherjee S, Sen R (2008b) Improved bioavailability and biodeg- sulfide and iron sulfide precipitation by a newly isolated Desul-
radation of a model polyaromatic hydrocarbon by a biosurfactant fotomaculum species and its relation to nickel resistance. FEMS
producing bacterium of marine origin. Chemosphere 72(9):1229– Microbiol Ecol 14(2):121–132. https://​doi.​org/​10.​1111/j.​1574-​
1234. https://​doi.​org/​10.​1016/j.​chemo​sphere.​2008.​05.​015 6941.​1994.​tb000​99.x
Das PK, Das BP, Dash P (2021) Chromite mining pollution, envi- Gao J, Fan H, Liu WW, Yang Q (2022) A new 3D Sm (III) compound:
ronmental impact, toxicity and phytoremediation: a review. photocatalytic property and application in the treatment of osteo-
Environ Chem Lett 19(2):1369–1381. https://​doi.​org/​10.​1007/​ arthritis of the foot and ankle. Sci Adv Mater 14(2):344–349.
s10311-​020-​01102-w https://​doi.​org/​10.​1166/​sam.​2022.​4209
Daź W, Habrat W, Tymczyszyn J, Krupa K (2022) Cutting mechanics Gapusan RB, Balela MDL (2020) Adsorption of anionic methyl orange
when turning powder metallurgy produced nickel-cobalt base dye and lead (II) heavy metal ion by polyaniline-kapok fiber
alloy with a cubic Boron Nitride insert. Int J Sci Technol Res nanocomposite. Mater Chem Phys 243:122682. https://​doi.​org/​
Int J 16(4):163–175. https://​doi.​org/​10.​12913/​22998​624/​152525 10.​1016/j.​match​emphys.​2020.​122682
de Sa Costa HP, da Silva MGC, Vieira MGA (2021) Biosorption of Genchi G, Carocci A, Lauria G, Sinicropi MS, Catalano A (2020)
aluminum ions from aqueous solutions using non-conventional Nickel: human health and environmental toxicology. Int J Envi-
low-cost materials: a review. J Water Process Eng 40:101925. ron Res Public Health 17(3):679. https://​doi.​org/​10.​3390/​ijerp​
https://​doi.​org/​10.​1016/j.​jwpe.​2021.​101925 h1703​0679
Delgado A, Anselmo AM, Novais JM (1998) Heavy metal biosorption Georgieva VG, Gonsalvesh L, Tavlieva MP (2020) Thermodynam-
by dried powdered mycelium of Fusarium flocciferum. Water ics and kinetics of the removal of nickel (II) ions from aqueous
Environ Res 70(3):370–375. https://​doi.​org/​10.​2175/​10614​ solutions by biochar adsorbent made from agro-waste walnut
3098X​125019 shells. J Mol Liq 312:112788. https://​doi.​org/​10.​1016/j.​molliq.​
Dhandole LK, Kim SG, Bae HS, Ryu HI, Chung HS, Seo YS, Jang 2020.​112788
JS (2020) Simultaneous and synergistic effect of heavy metal Gheethi, A. A., Efaq, A. N., Mohamed, R. M., Abdel-Monem, M. O.,
adsorption on the enhanced photocatalytic performance of a Abdullah, A. H., & Amir Hashim, M. (2017) Bio-removal of
visible-light-driven RS-TONR/TNT composite. Environ Res Nickel ions by Sporosarcina pasteurii and Bacillus megaterium,
180:108651. https://​doi.​org/​10.​1016/j.​envres.​2019.​108651 a comparative study. In IOP Conference Series: Materials Sci-
Diab HM, Alkahtani MA, Ahmed AS, Khalil AM, Alshehri MA, ence and Engineering 226, 1, 012044 IOP Publishing. https://​
Ahmed MA, Ahmed AE (2020) Coexistence of diverse heavy doi.​org/​10.​1088/​1757-​899X/​226/1/​012044

13
Environmental Science and Pollution Research (2024) 31:40224–40244 40241

Gong Y, Zhao D, Wang Q (2018) An overview of field-scale stud- wastewater. Biosorption 18(69):70–116. https://​d oi.​o rg/​1 0.​
ies on remediation of soil contaminated with heavy metals and 5772/​intec​hopen.​77315
metalloids: technical progress over the last decade. Water Res Kang SY, Lee JU, Kim KW (2005) Metal removal from wastewater
147:440–460. https://​doi.​org/​10.​1016/j.​watres.​2018.​10.​024 by bacterial sorption: Kinetics and competition studies. Envi-
Gong Y, Chai M, Ding H, Shi C, Wang Y, Li R (2020) Bioaccu- ron Technol 26(6):615–624. https://​doi.​org/​10.​1080/​09593​330.​
mulation and human health risk of shellfish contamination to 2001.​96195​01
heavy metals and As in most rapid urbanized Shenzhen, China. Khadim HJ, Ammar SH, Ebrahim SE (2019) Biomineralization based
Environ Sci Pollut Res 27:2096–2106. https://​doi.​org/​10.​1007/​ remediation of cadmium and nickel contaminated wastewater
s11356-​019-​06580-2 by ureolytic bacteria isolated from barn horses soil. Environ
Guarín-Romero JR, Rodríguez-Estupiñán P, Giraldo L, Moreno-Piraján Technol Innov 14:100315. https://​doi.​org/​10.​1016/j.​eti.​2019.​
JC (2019) Simple and competitive adsorption study of nickel (II) 100315
and chromium (III) on the surface of the brown algae Durvillaea Khajavian M, Wood DA, Hallajsani A, Majidian N (2019) Simulta-
antarctica biomass. ACS omega 4(19):18147–18158. https://d​ oi.​ neous biosorption of nickel and cadmium by the brown algae
org/​10.​1021/​acsom​ega.​9b020​61 Cystoseria indica characterized by isotherm and kinetic mod-
Gupta VK, Rastogi A, Nayak A (2010) Biosorption of nickel onto els. Appl Biol Chem 62(1):1–12. https://​d oi.​o rg/​1 0.​1 186/​
treated alga (Oedogonium hatei): application of isotherm and s13765-​019-​0477-6
kinetic models. J Colloid Interface Sci 342(2):533–539. https://​ Khan MA, Ngo HH, Guo W, Liu Y, Chang SW, Nguyen DD et al
doi.​org/​10.​1016/j.​jcis.​2009.​10.​074 (2018) Can membrane bioreactor be a smart option for water
Han L, Li J, Xue Q, Chen Z, Zhou Y, Poon CS (2020) Bacterial-induced treatment? Bioresour Technol Rep 4:80–87. https://​doi.​org/​10.​
mineralization (BIM) for soil solidification and heavy metal 1016/j.​biteb.​2018.​09.​002
stabilization: a critical review. Sci Total Environ 746:140967. Kim IH, Choi JH, Joo JO, Kim YK, Choi JW, Oh BK (2015) Develop-
https://​doi.​org/​10.​1016/j.​scito​tenv.​2020.​140967 ment of a microbe-zeolite carrier for the effective elimination of
Hassard F, Biddle J, Cartmell E, Jefferson B, Tyrrel S, Stephenson T heavy metals from seawater. J Microbiol Biotechnol 25(9):1542–
(2015) Rotating biological contactors for wastewater treatment–a 1546. https://​doi.​org/​10.​4014/​jmb.​1504.​04067
review. Process Saf Environ Prot 94:285–306. https://​doi.​org/​10.​ Kour D, Rana KL, Yadav N, Yadav AN, Rastegari AA, Singh C et al
1016/j.​psep.​2014.​07.​003 (2019) Technologies for biofuel production: current develop-
Hernandez-Cruz L, Lapidus GT, Carrillo-Romo F (1998) Modelling ment, challenges, and future prospects. In: Prospects of renew-
of nickel permeation through a supported liquid membrane. able bioprocessing in future energy systems, vol 1-50. https://d​ oi.​
Hydrometallurgy 48(3):265–276. https://d​ oi.o​ rg/1​ 0.1​ 016/S ​ 0304-​ org/​10.​1007/​978-3-​030-​14463-0_1
386X(98)​00008-5 Kumar V, Dwivedi SK (2020) Multimetal tolerant fungus Aspergil-
Hoseinzadeh S, Shahabivand S, Aliloo AA (2017) Toxic metals accu- lus flavus CR500 with remarkable stress response, simultaneous
mulation in Trichoderma asperellum and T. harzianum. Micro- multiple metal/loid removal ability and bioremediation potential
biology 86(6):728–736. https://​doi.​org/​10.​1134/​S0026​26171​ of wastewater. EnvironTechnol Innov 20:101075. https://d​ oi.o​ rg/​
70600​66 10.​1016/j.​eti.​2020.​101075
Huang Y, Zeng X, Guo L, Lan J, Zhang L, Cao D (2018) Heavy metal Kumar V, Dwivedi SK (2021) Mycoremediation of heavy met-
ion removal of wastewater by zeolite-imidazolate frameworks. als: processes, mechanisms, and affecting factors. Environ
Sep Purif Technol 194:462–469. https://​doi.​org/​10.​1016/j.​sep- Sci Pollut Res 28(9):10375–10412. https://​doi.​org/​10.​1007/​
pur.​2017.​11.​068 s11356-​020-​11491-8
Iqbal M, Saeed A (2007) Production of an immobilized hybrid biosorbent Lenntech Water treatment & air purification, 1998. http://www.lenn-
for the sorption of Ni (II) from aqueous solution. Process Biochem tech.com /groundwater/nitrates.htm
42(2):148–157. https://​doi.​org/​10.​1016/j.​procb​io.​2006.​07.​022 Leong YK, Chang JS (2020) Bioremediation of heavy metals using
Islam MA, Angove MJ, Morton DW (2019) Macroscopic and mod- microalgae: recent advances and mechanisms. Bioresour Tech-
eling evidence for nickel (II) adsorption onto selected manganese nol 303:122886. https://​doi.​org/​10.​1016/j.​biort​ech.​2020.​122886
oxides and boehmite. J Water Process Eng 32:100964. https://d​ oi.​ Li J, Wang X, Zhao G, Chen C, Chai Z, Alsaedi A, Wang X (2018)
org/​10.​1016/j.​jwpe.​2019.​100964 Metal–organic framework-based materials: superior adsorbents
Jaffrè T, Reeves RD, Baker AJM, Schat H, van der Ent A (2018) The for the capture of toxic and radioactive metal ions. Chem Soc Rev
discovery of nickel hyperaccumulation in the New Caledonian 47(7):2322–2356. https://​doi.​org/​10.​1039/​C7CS0​0543A
tree Pycnandra acuminata 40 years on: An introduction to a Vir- Li PX, Yang AY, Xin L, Xue B, Yin CH (2022) Photocatalytic activ-
tual Issue. New Phytol218:397–400. https://d​ oi.o​ rg/1​ 0.3​ 390/i​ jerp​ ity and mechanism of C ­ u2+ doped ZnO nanomaterials. Sci Adv
h1703​0679 Mater 14(10):1599–1604. https://d​ oi.o​ rg/1​ 0.1​ 166/s​ am.2​ 022.4​ 363
Jin H, Wu Y, Li Y (2022) Adsorption of ­Cu2+ and ­Pb2+ from munici- Lim HS, Lee JS, Chon HT, Sager M (2008) Heavy metal contamina-
pal wastewater by intercalation polymerization modified kao- tion and health risk assessment in the vicinity of the abandoned
lin. Sci Adv Mater 14(10):1589–1598. https://​doi.​org/​10.​1166/​ Songcheon Au–Ag mine in Korea. J Geochem Explor 96(2-3,
sam.​2022.​4350 223):–230. https://​doi.​org/​10.​1016/j.​gexplo.​2007.​04.​008
Joho M, Ishikawa Y, Kunikane M, Inouhe M, Tohoyama H, Muray- Liu X, Lu Z (2022) Simulation and optimization of the combined
ama T (1992) The subcellular distribution of nickel in Ni-sen- high-gradient magnetic separation-ultraviolet photocatalysis
sitive and Ni-resistant strains of Saccharomyces cerevisiae. (HGMS-UV/TiO2) system for ballast water treatment. Sci Adv
Microbios 71(287):149–159. https://​doi.​org/​10.​1111/j.​1432-​ Mater 14(4):710–717. https://​doi.​org/​10.​1166/​sam.​2022.​4259
1033.​1992.​tb169​20.x Liu X, Jiang B, Yin X, Ma H, Hsiao BS (2020) Highly permeable
Kamran MA, Eqani SAMAS, Bibi S, Xu RK, Monis MFH, Kat- nanofibrous composite microfiltration membranes for removal
soyiannis A, Chaudhary HJ (2016) Bioaccumulation of nickel of nanoparticles and heavy metal ions. Sep Purif Technol
by E. sativa and role of plant growth promoting rhizobacteria 233:115976. https://​doi.​org/​10.​1016/j.​seppur.​2019.​115976
(PGPRs) under nickel stress. Ecotoxicol Environ Saf 126:256– López A, Lázaro N, Morales S, Marqués AM (2002) Nickel biosorption
263. https://​doi.​org/​10.​1016/j.​ecoenv.​2016.​01.​002 by free and immobilized cells of Pseudomonas fluorescens 4F39:
Kanamarlapudi SLRK, Chintalpudi VK, Muddada S (2018) Appli- a comparative study. Water Air Soil Pollut 135:157–172. https://​
cation of biosorption for removal of heavy metals from doi.​org/​10.​1023/A:​10147​06827​124

13
40242 Environmental Science and Pollution Research (2024) 31:40224–40244

Lu F, Astruc D (2018) Nanomaterials for removal of toxic elements Priya AK, Gnanasekaran L, Dutta K, Rajendran S, Balakrishnan D,
from water. Coord Chem Rev 356:147–164. https://​doi.​org/​10.​ Soto-Moscoso M (2022) Biosorption of heavy metals by micro-
1016/j.​ccr.​2017.​11.​003 organisms: evaluation of different underlying mechanisms. Che-
Ma Y, Prasad MNV, Rajkumar M, Freitas HJBA (2011) Plant growth mosphere 307:135957. https://​doi.​org/​10.​1016/j.​chemo​sphere.​
promoting rhizobacteria and endophytes accelerate phytoreme- 2022.​135957
diation of metalliferous soils. Biotechnol Adv 29(2):248–258. Priyadarshanee M, Das S (2021) Biosorption and removal of toxic
https://​doi.​org/​10.​1016/j.​biote​chadv.​2010.​12.​001 heavy metals by metal tolerating bacteria for bioremediation of
Machalová L, Pipíška M, Trajteľová Z, Horník M (2015) Comparison metal contamination: a comprehensive review. J Environ Chem
of ­Cd2+ biosorption and bioaccumulation by bacteria–a radio- Eng 9(1):104686. https://​doi.​org/​10.​1016/j.​jece.​2020.​104686
metric study. https://​doi.​org/​10.​1515/​nbec-​2015-​0024 Qiu M, He C (2019) Efficient removal of heavy metal ions by forward
Marin NM (2022) Maize stalk obtained after acid treatment and its osmosis membrane with a polydopamine modified zeolitic imi-
use for simultaneous removal of ­Cu2+, ­Pb2+, ­Ni2+, ­Cd2+, ­Cr3+ dazolate framework incorporated selective layer. J Hazard Mater
and ­Fe3+. Polymers 14(15):3141. https://​doi.​org/​10.​3390/​polym​ 367:339–347. https://​doi.​org/​10.​1016/j.​jhazm​at.​2018.​12.​096
14153​141 Qu J, Wang Y, Tian X, Jiang Z, Deng F, Tao Y, Zhang Y (2021)
Marques AP, Rangel AO, Castro PM (2009) Remediation of heavy KOH-activated porous biochar with high specific surface area
metal contaminated soils: phytoremediation as a potentially for adsorptive removal of chromium (VI) and naphthalene from
promising clean-up technology. Crit Rev Environ Sci Technol water: affecting factors, mechanisms and reusability exploration.
39(8):622–654. https://​doi.​org/​10.​1080/​10643​38070​17982​72 J Hazard Mater 401:123292. https://​doi.​org/​10.​1016/j.​jhazm​at.​
Masindi V, Muedi KL (2018) Environmental contamination by heavy 2020.​123292
metals. Heavy metals 10:115–132. https://​doi.​org/​10.​5772/​intec​ Ramadoss R, Subramaniam D (2019) Removal of divalent nickel from
hopen.​76082 aqueous solution using blue-green marine algae: adsorption
Mattuschka B, Straube G (1993) Biosorption of metals by a waste modeling and applicability of various isotherm models. Sep Sci
biomass. J Chem Technol Biotechnol 58(1):57–63. https://​doi.​ Technol 54(6):943–961. https://d​ oi.o​ rg/1​ 0.1​ 080/0​ 14963​ 95.2​ 018.​
org/​10.​1002/​jctb.​28058​0108 15261​94
Middleton H, Yergeau É, Monard C, Combier JP, El Amrani A (2021) Rana S, Gupta N, Rana RS (2018) Removal of organic pollutant with
Rhizospheric plant–microbe interactions: miRNAs as a key the use of rotating biological contactor. Mater Today: Proc
mediator. Trends Plant Sci 26(2):132–141. https://​doi.​org/​10.​ 5(2):4218–4224. https://​doi.​org/​10.​1016/j.​matpr.​2017.​11.​685
1016/j.​tplan​ts.​2020.​09.​005 Rao KM, Sresty TVS (2000) Antioxidative parameters in the seedlings
Mishra A, Malik A (2013) Recent advances in microbial metal bioac- of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to
cumulation. Crit Rev Environ Sci Technol 43(11):1162–1222. Zn and Ni stresses. Plant Sci 157(1):113–128. https://​doi.​org/​
https://​doi.​org/​10.​1080/​10934​529.​2011.​627044 10.​1016/​S0168-​9452(00)​00273-9
Molina-Campos DF, Vargas Delgadillo DP, Giraldo L, Moreno-Piraján Ren Q, Chen P, Yang Y, Wei F, Chen H, Wang S, Liang Z (2023) Syn-
JC (2020) Removal of metal ions Cd (II), Cr (VI) and Ni (II) thesis of metal–organic frameworks for the adsorption of Congo
from aqueous solution using an organic aerogel and carbon aero- Red from wastewater. Sci Adv Mater 15:1159–1165
gel obtained by acid catalysis. Mater Express 10(1):127–139. Renu K, Chakraborty R, Myakala H, Koti R, Famurewa AC, Mad-
https://​doi.​org/​10.​1166/​mex.​2020.​1623 hyastha H, Gopalakrishnan AV (2021) Molecular mechanism
Naz M, Ghani MI, Sarraf M, Liu M, Fan X (2022) Ecotoxicity of nickel of heavy metals (lead, chromium, arsenic, mercury, nickel and
and its possible remediation. In: Phytoremediation. Academic cadmium)-induced hepatotoxicity–a review. Chemosphere
Press, pp 297–322. https://​doi.​org/​10.​1016/​B978-0-​323-​89874- 271:129735. https://d​ oi.o​ rg/1​ 0.1​ 016/j.c​ hemos​ phere.2​ 021.1​ 29735
4.​00022-4 Riekkola-Vanhanen M (2013) Talvivaara mining company–from a
Niec JH, Cha DK (2000) Influence of anoxic selectors on heavy metal project to a mine. Miner Eng 48:2–9. https://​doi.​org/​10.​1016/j.​
removal by activated sludge. Biotechnol Bioprocess Eng 5:431– mineng.​2013.​04.​018
435. https://​doi.​org/​10.​1007/​BF029​31943 Rodríguez CE, Quesada A (2006) Nickel biosorption by Acinetobacter
Niyonzima FN, Mahnashi MH, Shaikh IA, Mannasaheb BA, Gho- baumannii and Pseudomonas aeruginosa isolated from indus-
neim MM, Asdaq SM, Khan AA, Nsanganwimana F, More VS, trial wastewater. Braz J Microbiol 37:465–467. https://​doi.​org/​
Nuwayo SI, More SS (2023) Detergent-compatible amylases 10.​1590/​S1517-​83822​00600​04000​12
produced by fungal species and their applications in detergent Romera E, González F, Ballester A, Blázquez ML, Munoz JA (2007)
industry. Sci Adv Mater 15(5):607–616. https://​doi.​org/​10.​1166/​ Comparative study of biosorption of heavy metals using different
sam.​2023.​4476 types of algae. Bioresour Technol 98(17):3344–3353. https://d​ oi.​
Noormohamadi HR, Fat'hi MR, Ghaedi M, Ghezelbash GR (2019) org/​10.​1016/j.​biort​ech.​2006.​09.​026
Potentiality of white-rot fungi in biosorption of nickel and cad- Ruotolo R, Marchini G, Ottonello S (2008) Membrane transporters and
mium: modeling optimization and kinetics study. Chemosphere protein traffic networks differentially affecting metal tolerance:
216:124–130. https://​doi.​org/​10.​1016/j.​chemo​sphere.​2018.​10.​ a genomic phenotyping study in yeast. Genome Biol 9(4):R67.
113 https://​doi.​org/​10.​1186/​gb-​2008-9-​4-​r67
Orji OU, Awoke JN, Aja PM, Aloke C, Obasi OD, Alum EU et al Salgot M, Folch M (2018) Wastewater treatment and water reuse. Curr
(2021) Halotolerant and metalotolerant bacteria strains with Opin Environ Sci Health 2:64–74. https://​doi.​org/​10.​1016/j.​
heavy metals biorestoration possibilities isolated from Uburu coesh.​2018.​03.​005
Salt Lake, Southeastern, Nigeria. Heliyon 7(7):e07512. https://​ Sar P, Kazy SK, Singh SP (2001) Intracellular nickel accumulation
doi.​org/​10.​1016/j.​heliy​on.​2021.​e07512 by Pseudomonas aeruginosa and its chemical nature. Lett Appl
Öztürk A (2007) Removal of nickel from aqueous solution by the bac- Microbiol 32:257–261. https://​doi.​org/​10.​1046/j.​1472-​765x.​
terium Bacillus thuringiensis. J Hazard Mater 147(1-2):518–523. 2001.​00878.x
https://​doi.​org/​10.​1016/j.​jhazm​at.​2007.​01.​047 Sathyavathi S, Manjula A, Rajendhran J, Gunasekaran P (2014) Extra-
Pang FM, Kumar P, Teng TT, Omar AM, Wasewar KL (2011) Removal cellular synthesis and characterization of nickel oxide nanopar-
of lead, zinc and iron by coagulation–flocculation. J Taiwan Inst ticles from Microbacterium sp. MRS-1 towards bioremediation
Chem Eng 42(5):809–815. https://​doi.​org/​10.​1016/j.​jtice.​2011.​ of nickel electroplating industrial effluent. Bioresour Technol
01.​009 165:270–273. https://​doi.​org/​10.​1016/j.​biort​ech.​2014.​03.​031

13
Environmental Science and Pollution Research (2024) 31:40224–40244 40243

Semerjian L (2018) Removal of heavy metals (Cu, Pb) from aqueous Suo S, Gao J, Li J, Hu Y, Wang C, Deng R, Chen S (2022) 3D Cd
solutions using pine (Pinus halepensis) sawdust: equilibrium, (II)-based complex with photocatalytic property and treatment
kinetic, and thermodynamic studies. Environ Technol Innov activity on endometrial cancer. Sci Adv Mater 14(2):338–343.
12:91–103. https://​doi.​org/​10.​1016/j.​eti.​2018.​08.​005 https://​doi.​org/​10.​1166/​sam.​2022.​4208
Seregin I, Kozhevnikova AD (2006) Physiological role of nickel and its Talaee Shoar F, Delavari H, H., & Poursalehi, R. (2022) Kinetic, equi-
toxic effects on higher plants. Russ J Plant Physiol 53:257–277. librium, and thermodynamic studies for adsorptive removal of
https://​doi.​org/​10.​1134/​S1021​44370​60201​78 nickel ions by thermally modified diatomite from aqueous solu-
Seregin IV, Kozhevnikova AD, Kazyumina EM, Ivanov VB (2003) tion. Emergent Mater 5(2):401–412. https://​doi.​org/​10.​1007/​
Nickel toxicity and distribution in maize roots. Russ J Plant s42247-​022-​00380-0
Physiol 50(5). https://​doi.​org/​10.​1023/A:​10256​60712​475 Tang J, Wang Y, Song M, Ma S, Deng D (2022a) Comparative genomes
Shaikh IA, Muddapur UM, Srikanth B, Kulkarni MA, Krithika C, analysis of aflatoxin B1-degrading Pseudomonas strains with dif-
Mahnashi MH, Mannasaheb BA, Alsaikhan F, Khan AA, Iqubal ferent degradation Abilities. Sci Adv Mater 14(1):111–121
SM, Bahafi A (2022) In silico approach in targeting SARS- Tang SL, Liu YL, Li XM, Chen QW, Chen HY, Zhou JL, Chen L, Gu
CoV-2 virus protein Mpro using fungal metabolites. Sci Adv ZY, Shao SX, Qiao PZ, Shen GD (2022b) A novel core–shell
Mater 14(1):43–54. https://​doi.​org/​10.​1166/​sam.​2022.​4185 structure ­TiO2 nanolayer sphere preparation and electrocatalytic
Shamshad I, Khan S, Waqas M, Asma M, Nawab J, Gul N, Li G (2016) degradation study. Sci Adv Mater 14(3):576–580
Heavy metal uptake capacity of fresh water algae (Oedogonium Taran M, Sisakhtnezhad S, Azin T (2015) Biological removal of nickel
westti) from aqueous solution: a mesocosm research. Int J Phy- (II) by sp. KL1 in different conditions: optimization by Taguchi
toremediation 18(4):393–398. https://d​ oi.o​ rg/1​ 0.1​ 080/1​ 52265​ 14.​ statistical approach. Polish J Chem Technol 17(3):29–32. https://​
2015.​11095​94 doi.​org/​10.​1515/​pjct-​2015-​0046
Shamshad I, Khan S, Muhammad S, Waqas M (2020) Unreveal- Taştan BE, Ertuğrul S, Dönmez G (2010) Effective bioremoval of reac-
ing the biosorption capacity of freshwater algae biomasses tive dye and heavy metals by Aspergillus versicolor. Bioresour
for toxic heavy metals in aqueous solutions. Desalin Water Technol 101(3):870–876. https://​doi.​org/​10.​1016/j.​biort​ech.​
Treat 184:189–198 2009.​08.​099
Sharma KR, Naruka A, Raja M, Sharma RK (2022) White rot fungus Topare NS, Wadgaonkar VS (2022) A review on application of low-
mediated removal of mercury from wastewater. Water Environ cost adsorbents for heavy metals removal from wastewater. Mater
Res 94(7):e10769. https://​doi.​org/​10.​1002/​wer.​10769 Today: Proc https://​doi.​org/​10.​1016/j.​matpr.​2022.​08.​450
Shen Y, Sun P, Ye L, Xu D (2023) Progress of anaerobic mem- Tripathi VN, Srivastava S (2006) Extracytoplasmic storage as the
brane bioreactor in municipal wastewater treatment. Sci Adv nickel resistance mechanism in a natural isolate of Pseudomonas
Mater:1277–1298 putida S4. Can J Microbiol 52:287–292. https://​doi.​org/​10.1​ 139/​
Shi Y, Zhang T, Ren H, Kruse A, Cui R (2018) Polyethylene imine w05-​133
modified hydrochar adsorption for chromium (VI) and nickel (II) Verma B, Balomajumder C (2020) Surface modification of one-dimen-
removal from aqueous solution. Bioresour Technol 247:370–379. sional carbon nanotubes: a review for the management of heavy
https://​doi.​org/​10.​1016/j.​biort​ech.​2017.​09.​107 metals in wastewater. Environ Technol Innov 17:100596. https://​
Shinde NR, Bankar AV, Kumar AR, Zinjarde SS (2012) Removal of Ni doi.​org/​10.​1016/j.​eti.​2019.​100596
(II) ions from aqueous solutions by biosorption onto two strains Verma S, Kuila A (2019) Bioremediation of heavy metals by microbial
of Yarrowia lipolytica. J Environ Manag 102:115–124. https://​ process. Environ Technol Innov 14:100369. https://​doi.​org/​10.​
doi.​org/​10.​1016/j.​jenvm​an.​2012.​02.​026 1016/j.​eti.​2019.​100369
Siddiquee S, Aishah SN, Azad SA, Shafawati SN, Naher L (2013) Walker CD, Graham RD, Madison JT, Cary EE, Welch RM (1985)
Tolerance and biosorption capacity of Zn 2+, Pb 2+, Ni 3+ and Cu Effects of Ni deficiency on some nitrogen metabolites in cow-
2+
by filamentous fungi (Trichoderma harzianum, T. aureoviride peas (Vigna unguiculata L. Walp). Plant Physiol 79(2):474–479.
and T. virens). Adv Biosci Biotechnol 4(4): 70–583. https://​doi.​ https://​doi.​org/​10.​1104/​pp.​79.2.​474
org/​10.​4236/​abb.​2013.​44075 Wang HK, Wood JM (1984) Bioaccumulation of nickel by algae. Envi-
Singh G, Dwivedi SK (2020) Decolorization and degradation of Direct ron Sci Technol 18(2):106–109. https://​doi.​org/​10.​1021/​es001​
Blue-1 (Azo dye) by newly isolated fungus Aspergillus terreus 20a011
GS28, from sludge of carpet industry. Environ Technol Innov Wang K (2023) Application of green pollution-free materials in envi-
18:100751. https://​doi.​org/​10.​1016/j.​eti.​2020.​100751 ronmental art design. Sci Adv Mater 15(1):41–49. https://​doi.​
Singh N, Kumar A, Sharma B (2019) Role of fungal enzymes for biore- org/​10.​1166/​sam.​2023.​4427
mediation of hazardous chemicals. In: Recent Advancement in Wang H, Wang X, Xu J, Zhang Y (2022) Environmental impact of
White Biotechnology Through Fungi: Volume 3: Perspective for construction waste mixture containing heavy metals pollutants
Sustainable Environments, pp 237–256. https://​doi.​org/​10.​1007/​ cadmium (Cd) and ARSENIC (As) used in highway engineer-
978-3-​030-​25506-0_9 ing. Sci Adv Mater 14(7):1159–1165. https://​doi.​org/​10.​1166/​
Sulaymon AH, Mohammed AA, Al-Musawi TJ (2013) Competitive sam.​2022.​4299
biosorption of lead, cadmium, copper, and arsenic ions using Wei H, Fang Y, Mulligan P, Chuirazzi W, Fang HH, Wang C et al
algae. Environ Sci Pollut Res 20:3011–3023. https://​doi.​org/​ (2016) Sensitive X-ray detectors made of methylammonium lead
10.​1007/​s11356-​012-​1208-2 tribromide perovskite single crystals. Nat Photonics 10(5):333–
Sun Q, Wang W, Yang L, Huang S, Xu Z, Ji Z, Hu Y (2018) Sepa- 339. https://​doi.​org/​10.​1038/​nphot​on.​2016.​41
ration and recovery of heavy metals from concentrated smelt- Wierzba S (2015) Biosorption of lead (II), zinc (II) and nickel (II)
ing wastewater by synergistic solvent extraction using a mix- from industrial wastewater by Stenotrophomonas maltophilia and
ture of 2-hydroxy-5-nonylacetophenone oxime and bis (2, 4, Bacillus subtilis. Pol J Chem Technol 17(1):79–87. https://​doi.​
4-trimethylpentyl)-phosphinic acid. Solvent Extr Ion Exch org/​10.​1515/​pjct-​2015-​0012
36(2):175–190. https://d​ oi.o​ rg/1​ 0.1​ 080/0​ 73662​ 99.2​ 018.1​ 44668​ 0 Wierzba S (2017) Biosorption of nickel (II) and zinc (II) from aqueous
Sundararaju S, Manjula A, Kumaravel V, Muneeswaran T, Vennila T solutions by the biomass of yeast Yarrowia lipolytica. Pol J Chem
(2020) Biosorption of nickel ions using fungal biomass Penicil- Technol 19(1):1–10. https://​doi.​org/​10.​1515/​pjct-​2017-​0001
lium sp. MRF1 for the treatment of nickel electroplating indus- Wong JPK, Wong YS, Tam NFY (2000) Nickel biosorption by two
trial effluent. Biomass Convers Biorefin 12:1059–1068 chlorella species, C. Vulgaris (a commercial species) and C.

13
40244 Environmental Science and Pollution Research (2024) 31:40224–40244

Miniata (a local isolate). Bioresour Technol 73(2):133–137. Zaidi S, Usmani S, Singh BR, Musarrat J (2006) Significance of Bacil-
https://​doi.​org/​10.​1016/​S0960-​8524(99)​00175-3 lus subtilis strain SJ-101 as a bioinoculant for concurrent plant
Wong S, Ngadi N, Inuwa IM, Hassan O (2018) Recent advances in growth promotion and nickel accumulation in Brassica juncea.
applications of activated carbon from biowaste for wastewater Chemosphere 64(6):991–997. https://​doi.​org/​10.​1016/j.​chemo​
treatment: a short review. J Clean Prod 175:361–375. https://​doi.​ sphere.​2005.​12.​057
org/​10.​1016/j.​jclep​ro.​2017.​12.​059 Zeng SL, Zhou L, Liu XX (2022) A new photoactive Cd (II) MOF:
Wu X, Huang P, Dong C, Deng X (2021) Nickel bioaccumulation by a dye degradation and nursing values on postpartum infection by
marine bacterium Brevibacterium sp.(X6) isolated from Shenz- inhibiting the Staphylococcus aureus growth. Sci Adv Mater
hen Bay, China. Mar Pollut Bull 170:112656. https://​doi.​org/​10.​ 14(7):1277–1283. https://​doi.​org/​10.​1166/​sam.​2022.​4275
1016/j.​marpo​lbul.​2021.​112656 Zhang L, Angle JS, Chaney R (2007) Do high-nickel leaves shed by the
Xu Z, Song X, Li Y, Li G, Luo W (2019) Removal of antibiotics by nickel hyperaccumulator Alyssum murale inhibit seed germina-
sequencing-batch membrane bioreactor for swine wastewater tion of competing plants? New Phytol 173(3):509–516. https://​
treatment. Sci Total Environ 684:23–30. https://​doi.​org/​10.​ doi.​org/​10.​1111/j.​1469-​8137.​2006.​01952.x
1016/j.​scito​tenv.​2019.​05.​241 Zhou W, Lan B, Liu Q, Li Z (2023) Effect of polyamidoamine-den-
Yadav KK, Gupta N, Kumar A, Reece LM, Singh N, Rezania S, Khan drimer nanoparticles combined with human umbilical vein
SA (2018) Mechanistic understanding and holistic approach of endothelial cell microenvironment on the growth and immune
phytoremediation: a review on application and future prospects. infiltration of nasopharyngeal carcinoma cell line CNE-1. Sci
Ecol Eng 120:274–298. https://​doi.​org/​10.​1016/j.​ecole​ng.​2018.​ Adv Mater 15:1224–1233
05.​039 Zouboulis AI, Loukidou MX, Matis KA (2004) Biosorption of toxic
Yang C, Qin W, Lai S, Wang J, Zhang Y, Jiao F et al (2011) Bioleach- metals from aqueous solutions by bacteria strains isolated from
ing of a low grade nickel–copper–cobalt sulfide ore. Hydrometal- metal-polluted soils. Process Biochem 39(8):909–916. https://​
lurgy 106(1-2):32–37. https://​doi.​org/​10.​1016/j.​hydro​met.​2010.​ doi.​org/​10.​1016/​S0032-​9592(03)​00200-0
11.​013
Yang J, Zhu G, Nie L, Li G, Wu W, Wang B (2022) Treatment of heavy- Publisher’s note Springer Nature remains neutral with regard to
metal-containing oily wastewater using a novel α-zirconium- jurisdictional claims in published maps and institutional affiliations.
phosphate/polyacrylonitrile ultrafiltration membrane. Sci Adv
Mater 14(4):644–654 Springer Nature or its licensor (e.g. a society or other partner) holds
Yang D, Chen SK, Xu CH, Zhou Z (2023) Study on adsorption of exclusive rights to this article under a publishing agreement with the
phosphate in water environment by Mg–Al modified biochar. Sci author(s) or other rightsholder(s); author self-archiving of the accepted
Adv Mater 15(6):807–817 manuscript version of this article is solely governed by the terms of
Yin K, Wang Q, Lv M, Chen L (2019) Microorganism remediation such publishing agreement and applicable law.
strategies towards heavy metals. Chem Eng J 360:1553–1563.
https://​doi.​org/​10.​1016/j.​cej.​2018.​10.​226

13

You might also like