Environmental Technology & Innovation: Uday Kumar Banala, Nilamadhab Prasad Indradyumna Das, Subba Rao Toleti

Environmental Technology & Innovation xxx (xxxx) xxx
Contents lists available at ScienceDirect
Environmental Technology & Innovation

journal homepage: www.elsevier.com/locate/eti
Microbial interactions with uranium: Towards an effective

bioremediation approach
Uday Kumar Banala a,b , Nilamadhab Prasad Indradyumna Das a ,
∗
Subba Rao Toleti b,c ,
a
Radiological and Environmental Safety Division, Indira Gandhi Centre for Atomic Research, Kalpakkam 603102, India
b
Homi Bhabha National Institute, Anushakti Nagar, Mumbai 400094, India
c
Water and Steam Chemistry Division, Chemistry Group, Bhabha Atomic Research Centre, Kalpakkam 603102, India
article info a b s t r a c t
Article history: In uranium bioremediation, the response of different biological groups towards uranium
Received 6 July 2020 are critical. Understanding the metal–microbe interactions would provide adequate
Received in revised form 23 September 2020 knowledge to develop the remediation technique. Owing to this application, many
Accepted 7 November 2020
studies have been reported on various strategies using different microbial agents. These
Available online xxxx
microorganisms can adsorb, accumulate, reduce, or mineralize uranium as a survival
Keywords: mechanism. This review is intended to discuss the plausible uranium–microbial inter-
Uranium actions that could sequester and limit the uranium contamination in the environment. A
Biosorption detailed description of the key processes such as biosorption, biomineralization, biore-
Bioprecipitation duction and bioaccumulation of uranium by various biological groups are provided in
Bioreduction
this review. Concise information about the uranium speciation and other environmental
Bioaccumulation
factors which can substantially influence the in situ bioremediation are also discussed.
Chemical methods
Finally, a comparative assessment of chemical methods versus biological procedures in
the remediation of uranium was explained. This review brings out the importance of
the various biological agents and factors associated with the bioremediation of uranium
contaminated sites.
© 2020 Elsevier B.V. All rights reserved.
Contents
1. Introduction............................................................................................................................................................................................... 2
2. Chemical methods for uranium sequestration...................................................................................................................................... 2
3. Microbial interactions with uranium ..................................................................................................................................................... 3
3.1. Biosorption .................................................................................................................................................................................. 3
3.2. Biomineralization ........................................................................................................................................................................ 7
3.3. Bioreduction ................................................................................................................................................................................ 9
3.4. Bioaccumulation ......................................................................................................................................................................... 10
4. Conclusion ................................................................................................................................................................................................. 11
Declaration of competing interest.......................................................................................................................................................... 11
Acknowledgement .................................................................................................................................................................................... 11
References ................................................................................................................................................................................................. 12
∗ Corresponding author at: Water and Steam Chemistry Division, Chemistry Group, Bhabha Atomic Research Centre, Kalpakkam 603102, India.
E-mail address: subbarao@igcar.gov.in (S.R. Toleti).
https://doi.org/10.1016/j.eti.2020.101254
2352-1864/© 2020 Elsevier B.V. All rights reserved.
Please cite this article as: U.K. Banala, N.P.I. Das and S.R. Toleti, Microbial interactions with uranium: Towards an effective bioremediation approach.
Environmental Technology & Innovation (2020) 101254, https://doi.org/10.1016/j.eti.2020.101254.
U.K. Banala, N.P.I. Das and S.R. Toleti Environmental Technology & Innovation xxx (xxxx) xxx
1. Introduction
Environmental contamination with uranium or other radionuclides has posed a significant problem owing to its radi-
ological and chemical toxicity. Anthropogenic activities such as mineral mining, nuclear weapon testing, and utilization
of uranium-containing phosphate fertilizers and natural leaching of uranium bearing rocks have resulted in increased
distribution of uranium in the environment (Todorov, 2004). Uranium (U) is a naturally occurring radioactive element
found in various physical and chemical forms in the earth crust with a specific density of 19 g/cm3 . In nature, uranium
exists as complex ores as pitchblende, uraninite, carnotite, autunite, uranophane, and torbernite. Uraninite or pitchblende
is the primary mineral of uranium comprising of approximately 50%–80% of its total ore (Choppin et al., 2013; Francis,
1994). Earth crust contains approximately 2.8 mg U/kg. In river water, the concentration of uranium is 0.01–6.6 µg/L,
while 30 µg/L and 3.32 µg/L are reported in groundwater and seawater, respectively (Markich, 2002). However, due to
various anthropogenic activities, high concentrations of uranium have been reported in certain places. For instance, in the
USA, concentrations of uranium as high as 11.7 g/L in groundwater and 16 mg/g in soil and sediment samples have been
reported. A nuclear waste storage site at Oak Ridge National Laboratory has 0.8 mg U/g (Kolhe et al., 2018). Similarly, in
India, the concentration of uranium in drinking water wells was found to surpass the WHO guidelines limit of 30 µg/L
(WHO, 2011; Coyte et al., 2018).
Both biochemical and radiological effects of uranium isotopes and its progenies pose toxicity to humans and other
organisms. In this case, chemical toxicity is more prevalent than radiotoxicity. Uranium exists in different oxidation states
ranging from +2 to +6. Under oxidizing conditions and at pH ≤ 2.5, it exists as mobile U (VI) wherein uranyl ion (UO2 2+ )
is the prevalent ion and is known to be soluble and more toxic. In reducing conditions, insoluble and immobile uraninite
(UO2 )[s] form predominates and is less toxic. Uranium released into the environment enters aquatic and terrestrial
organisms through the food chains (Anke et al., 2009). Once uranium enters the blood, it forms various complexes like
uranyl bis- and tris-carbonate complexes and UO2 -protein complexes with human serum albumin, transferrin, and other
proteins. Uranium has a high binding affinity towards phosphate groups and binds to phosphorylated peptides (Pardoux
et al., 2012). In vivo studies have shown that the uranyl cation is the dominant form and is known to damage the kidneys
(acts as a nephrotoxin) (Anke et al., 2009). Moreover, the radiation energy deposited inside the organism can cause DNA
damage leading to cancer (Mukherjee et al., 2012; Park and Jiao, 2014). Similarly, depleted uranium (DU) is also a health
hazard (Briner, 2010). DU arises as a by-product during the production of enriched uranium. While, in microorganisms,
uranium toxicity leads to decreased cell viability, metabolic activity, and increased DNA damage (Sepulveda-Medina et al.,
2015; Park and Jiao, 2014). It has also been reported that uranium toxicity caused increased membrane permeability,
oxidative damage, and transient RNA degradation (Kolhe et al., 2020).
Apart from health issues to human beings, uranium contamination has many ecological consequences. Therefore, mon-
itoring and remediation of uranium contaminated sites become vital for environmental safety and regulatory compliance
guidelines. Hence, several physical and chemical methods are employed for the treatment of metal contaminated sites. On
the contrary, a more eco-friendly and economical method is the need of the hour, which is fulfilled by the microbiological
methods. Microbial interactions with the metal ions lead to change in concentration or oxidation, which controls the
mobility as well as bioavailability of the metal (Acharya, 2015). Numerous literature reports suggested that the indigenous
microbes from toxic metal-contaminated sites can have a higher tolerance to heavy metals and other toxic substances
(Islam and Sar, 2011; Pollmann et al., 2006). These microbes have developed various mechanisms to immobilize toxic
metals or radionuclides such as enzymatic precipitation, biosorption, bioaccumulation and redistribution of toxic metals
or radionuclides in a stable mineral phase. These unique properties of microorganisms can be utilized to clean up the
contaminated sites.
Previously, several reviews have discussed biological methods, conventional methods and biogeochemistry and biore-
mediation of uranium (Kolhe et al., 2018; Selvakumar et al., 2018; Newsome et al., 2014; Xie et al., 2019). However, to our
knowledge, the reviews discussing both chemical and biological methods for uranium sequestration are rare. Therefore,
we have addressed comprehensive details on uranium bioremediation concerning biological interactions and conventional
treatment methods. It encompasses the speciation and factors affecting the uranium bioremediation by biological agents
and their interactions. The advantages, disadvantages, and future applications of uranium bioremediation have been
elucidated. Finally, a comparative account of bioremediation with chemical methods is also presented for the benefit
of the readers.
2. Chemical methods for uranium sequestration
The primary objective of any remediation or treatment process is to ease the risks associated with contaminant to
the ecosystem. Generally, remediation technologies can be in situ or ex situ, and choice of the treatment depends on
various factors such as characteristics of sites, initial metal concentration, cost, feasibility, and environmental concerns
(Rajasulochana and Preethy, 2016). To meet the safety regulation guidelines and for environmental safety, various methods
of uranium remediation have been extensively studied, from conventional methods to advanced technologies. Some of the
methods include chemical precipitation (Baker et al., 2019), membrane separation (Kolev et al., 2013), solvent extraction
(Wang and Zhuang, 2019), electrochemical purification (Wei et al., 2016), reverse osmosis (Shen and Schäfer, 2014), ion
exchange (Khawassek et al., 2018) and adsorption (Sureshkumar et al., 2010). Some of the important methods, such as
solvent extraction and adsorption, are discussed below.
2
The solvent extraction process uses organophosphorus compounds, which have high affinity and good coordinating
ability towards uranyl ion. Some of the widely used organophosphorus compounds for the abstraction of uranium are
tributyl phosphate (TBP), octyl(phenyl)-N,N-di-isobutyl carbamoyl methylphosphine oxide (CMPO), trioctylphosphine
oxide (TOPO), dihexyl-N,N-di-ethylcarbamoyl- methylphosphonate (CMP), di-2-ethylhexyl phosphoric acid (D2EHPA),
monododecyl phosphoric acid (DDPA), dibutyl butyl phosphonate (DBBP) and glycerophosphate (Wang and Zhuang, 2019).
Among all the organophosphorus compounds studied, tributyl phosphate (TBP) is the commonly used and has been
commercialized for recovery of uranium from the spent nuclear fuels in the nuclear industry (PUREX process) (Lanham
and Runion, 1949). This solvent extraction process is considered as an appropriate method for selective separation of
uranyl ions from aqueous solutions. However, this has disadvantages like non-biodegradability of TBP, solvent loss and
generation of secondary waste, which require additional efforts for disposal (Gupta et al., 2018). In recent years amide
based green extraction solvents have been studied, and it could be considered as a substitute for the organophosphorus
compounds (Manchanda and Pathak, 2004). Similarly, solubilization using chelating agents like carbonates (Mason et al.,
1997) and citrate (Kantar and Honeyman, 2006) are also used to recover uranium. Citric acid is effectively applied for in
situ and ex situ extraction of soils and decontamination in the nuclear industry. One of the advantages of using citrate in
complexing uranium is the biodegradability of U-citrate complex as it does not release the uranium upon its degradation
(Huang et al., 1998).
Adsorption is widely studied, common and most efficient method for environmental remediation. The advantages
of adsorption-based technology are low cost, excellent stability, and ease of modification of functional groups for
higher adsorption capacity. For adsorption based environmental remediation various organic (resins, chitosan, cellulose,
polypropylene, and others), inorganic (silica, carbon nanotubes, graphene oxide) and hybrid (magnetic composites)
adsorbents have been synthesized and characterized (Abdi et al., 2017; Anirudhan and Sreekumari, 2010; Calì et al., 2018;
Christou et al., 2019; Guo et al., 2018; Khawassek et al., 2018; Qian et al., 2018; Vivero-Escoto et al., 2013). First-time
Polypyrroles have been used to remove the uranium, and it showed a maximum loading capacity of 87.72 mg U/g (Abdi
et al., 2017). Polymers serve as suitable adsorbents for removal of uranium as they provide excellent chemical stability and
ample functional groups. These can be used directly or could be chemically modified to enhance the complex formation
towards uranyl ion. Polyvinyl-pyrrolidone/chitosan blended nanofibrils have been synthesized and studied for uranyl
adsorption from aqueous solutions. This blended polymer has the extreme uranium loading capacity of 167 mg U/g and
can be used multiple times without loss in efficiency (Christou et al., 2019). Some of the polymer adsorbents that are used
to remove uranium are collagen immobilized tannins (Sun et al., 2010), titanium loaded collagen fibres (Cheng et al., 2011)
and alkali-activated collagen fibres (Deng et al., 2018). In recent years, a variety of sorbents have been synthesized and
studied for uranium sequestration. One of the highly efficient sorbents is titanium phosphate which has an extraordinary
sorption capacity of 1250 mg/g (Kapnisti et al., 2018). Recently, mesoporous silica (MCM-41) has been studied for uranium
sequestration which has a high Langmuir adsorption capacity of 1067 mg U/g at pH ≥ 6 and 680 mg U/g from seawater
(Amesh et al., 2020).
In recent years, many studies have reported on nanotechnology based remediation of the environment (Ngomsik
et al., 2005; Yantasee et al., 2007). Nanoparticles and nanotubes provide excellent stability; however, they will have
low adsorption capacity and selectivity towards the uranium. For example, a study by Das et al. (2010) has shown the
maximum loading capacity of only 5 mg U/g of nanoparticles. Functionalized nanoparticles can overcome this low loading
capacity of nanoparticles. In a recent study by Calì et al. (2018), functionalized magnetic nanoparticles with phosphate via
a ligand exchange reaction were used. These phosphate-Fe3 O4 nanoparticles have an extremely high loading capacity of
∼1700 mg U/g along with specificity and selectivity. Table 1 summarizes the adsorption capacities of different chemical
sorbents used for uranium sequestration.
Although synthesized sorbents yielded remarkable loading capacity and selectivity towards the metals, economic
viability is an essential factor to be considered for field applications. In this scenario, biologically derived adsorbents
would be superior as they are economical and biodegradable.
3. Microbial interactions with uranium
Biological agents such as bacteria, fungi or plants interact with the uranium in a variety of ways to protect and
survive in the environment containing naturally abundant uranium or contaminated sites (Merroun and Selenska-Pobell,
2008). A wide range of organisms has been identified and characterized from mining and contaminated sites that can
remove or immobilize the uranium. These interactions of biological agents with uranium results in the sequestration or
complexation and thereby decrease the concentration of toxic metal in the environment. The metal–microbe interactions
include biosorption, biomineralization, bioreduction and bioaccumulation. These methods are of great significance in
terms of bioremediation and are discussed in the following sections.
3.1. Biosorption
Sorption is a common term referred to both adsorption and absorption. However, adsorption is a two-dimensional
phenomenon, whereas absorption is a three-dimensional phenomenon. Adsorption is the traditionally used term in
treatment technologies, although it involves different other mechanisms. Biosorption is the amalgamation of sorption
3
Table 1
Performances of different chemical sorbents for uranium adsorption.
Sorbent pH Maximum loading capacity Ref.
(mg/g)
Phosphated- Fe3 O4 NPs 7.0 1690 Calì et al. (2018)
GO-COOH/UiO-66 8 1097 Yang et al. (2017)
Salicylaldoxime/polydopamine modified reduced graphene oxide 5 1049 Qian et al. (2018)
Fe3 O4 into calcium alginate coated chitosan HCl hydrogel beads 6.0 392.69 Yi et al. (2018)
α -aminophosphonate functionalized chitosan 5.0 245 Imam et al. (2018)
Chitosan-tripolyphosphate beads 5.0 236.9 Sureshkumar et al. (2010)
TBP-SBA-15 5 197.8 Xue et al. (2017)
Phosphoryl multiwalled carbon nanotubes (PS-MWCNTs) 5.0 194.17 Guo et al. (2018)
MSPh-III 8.3 185.2 Vivero-Escoto et al. (2013)
Polyvinylpyrrolidone/Chitosan blended nanofibers 6.0 167 Christou et al. (2019)
Tributyl PO4 -C nanotubes 5.0 166.7 Mishra et al. (2016)
Amidoxime-grafted multiwalled carbon nanotubes 4.5 145 Wang et al. (2014)
MMSNs-PPI 9.6 133.3 Li et al. (2016b, 2017b)
Amberjet 1200 H 1.2 133 Khawassek et al. (2018)
Amidoxime-SiO2 @ Fe3 O4 NPs 5.0 105 Zhao et al. (2014)
Zeolite X- PAN – 90 Akyil and Eral (2005)
Polypyrrole 5.0 87.72 Abdi et al. (2017)
Anionic resin Dowex A 3.9 79 Ladeira and Gonçalves (2007)
Graphene/ Fe3 O4 NPs 5.5 69.5 Zong et al. (2013)
Amidoxime (AO) modified multiwalled carbon nanotubes (MWCNT) 5.0 67.9 Wu et al. (2018)
Amidoxime modified chitosan/ bentonite composite 8.0 49.09 Anirudhan et al. (2019)
Chitosan modified multiwalled carbon nanotube 5.0 41 Chen et al. (2013)
MMSNs-PP 3.5 37.5 Li et al. (2016a,b, 2017a,b)
Gel-amide 7.0 28.98 Venkatesan et al. (2004)
Succinic acid impregnated amberlite XAD-4 4.5–8.0 12.33 Metilda et al. (2005)
Fe3 O4 NPs 7.0 5 Das et al. (2010)
technology with biological material and is defined as ‘‘the uptake of metal species by physicochemical mechanisms and is
independent of metabolic process’’ (Gadd, 2009). Although it is simple metabolism independent physicochemical process,
sometimes pre-growth conditions can affect the efficiency of biosorption, and metabolic activity may also affect the
process, e.g. by triggering localized changes in pH or by releasing metal complexing ligands (Gadd, 2004).
All biological moieties like bacteria, fungi, algae, plant, and animal biomass as well as derived products such as chitosan
have the capability of biosorption. Specific functional groups present on the cell surface such as carboxyl, amine, hydroxyl,
phosphate, and sulfhydryl groups interact with the metal and leads to the sorption of metals (Fowle et al., 2000; Gorman-
Lewis et al., 2005; Lütke et al., 2012). Gram-positive bacterial cell wall consists of a thick peptidoglycan layer with few
teichoic acids. Whereas, Gram-negative bacterial cell wall is more complicated due to the additional lipopolysaccharide
(LPS) membrane outside a thin peptidoglycan cell wall. Archea cell wall differs from the bacterial cell wall in lacking the
peptidoglycan, whereas cyanobacteria share a similar cell structure with the Gram-negative bacteria. Of this microbial
mediated remediation carboxyl groups in the peptidoglycan and the phosphoryl groups in the teichoic acids are the
most probable sites for the metal complexing (Merroun et al., 2005). Langley and Beveridge (1999) depicted the role
of carboxylic groups in the binding of metal cations to O-side-chains of LPS and inferred that metal was most likely to
bind to phosphoryl groups in the core-lipid ‘A’ of LPS (Fig. 1). The bacterial extracellular polymeric substances (EPS) can
also aid in sequestration of metal ions. For example, P. aeruginosa, A. ferroxidans, Myxococcus Xanthus and other strains
isolated from different habitats have exhibited the complexation of U within EPS (Beech and Cheung, 1995; Kazy et al.,
2008).
To date, several environmental bacterial isolates have been used to quantify the uranium binding capacity. Biosorption
capacities and characteristics of different biosorbents are presented in Table 2 (bacteria), Table 3 (fungi) and Table 4 (algae)
Table 5 (other biosorbents). From Table 2, it was observed that actinomycetes named Brachybaterium sp. G1, which was
isolated from the German salt dome Gorlebenhad showed the maximum biosorption capacity of 971 mg U/g biomass.
The process was complete biosorption, and carboxylic functional groups played a significant role in the interaction of
uranium with the bacterial cells (Bader et al., 2018). To improve the mechanical stability and efficiency, immobilized
biomass was used for uranium sequestration and proved to a viable option in various studies. For instance, Geobacillus
thermoleovorans sub sp stromboliensis was immobilized onto an Amberlite XAD-4 ion exchange resin and used for pre-
concentration of uranium in the solid-phase extractor (SPE) (Özdemir and Kilinc, 2012). Synechococcus elongatus cells
were immobilized in polyacrylamide gels and used for the removal of uranium in a continuous flow-through system.
This procedure had significant uranium binding capacity up to three adsorption–desorption cycles (Acharya and Apte,
2013a). The multiwalled carbon nanotubes (MWCNTs) were loaded with B. mojavensis and B. vallismortis and studied for
pre-concentration of uranium as SPE (Özdemir et al., 2017,a). The biosorption capacities of B. mojavensis and B. vallismortis
loaded MWCNTs were 25.8 and 23.6 mg U/g, respectively. They could be used in multiple adsorption–desorption cycles
without significant loss in biosorption efficiency. Similarly, in a recent study by Tong (2017) reported the immobilization
4
Fig. 1. Schematic representation of biosorption of uranium.
Table 2
Uranium biosorption capacities of different bacteria.
Name of organism Biomass quantity Uranium concentration pH Loading capacity Ref.
(mg) (mg/g)
Brachybacterium sp. G1 – 0.04 mM 6.0 971 Bader et al. (2018)
Bacillus subtilis (alginate-chitosan – 150 mg/L 6.0 376.64 Tong (2017)
microcapsules)
Pseudomonas aeruginosa CSU 30–50 0.4 mM 2.4 100 Strandberg et al. (1981)
Anabaena torulosa – 0.1 mM 7.8 77.35 Acharya et al. (2012) and
Acharya and Apte (2013b)
Synechococcus elongatus – 1 mM 7.8 72.5 Acharya and Apte (2013a)
(immobilized)
Synechococcus elongatus – 0.1 mM 7.8 53.5 Acharya et al. (2009)
Citrobacter freudii – 0.084–0.63 mM – 48 Xie et al. (2008)
Microcystis aeruginosa – 0.168 mM 7.0 44 Li et al. (2004)
Amycolatopsis sp. K47 0.001 0.168 mM 4.0 38.8 Celik et al. (2018)
Myxococcus xanthus 20 1 mM 4.5 28.56 Gonzälez-Muñoz et al. (1997)
Bacillus mojavencis (carbon nanotubes 20 10 mg/L 5.0 25.8 Özdemir et al. (2017a)
loaded)
Bacillus vallismortis (carbon 50 10 mg/L 5.0 23.6 Özdemir et al. (2017)
nanotubes loaded)
Geobacillus Thermoleovorans subsp. 250 4.20 mM 5.0 11 Özdemir and Kilinc (2012)
Stromboliensis (immobilized
AmberliteXAD-4 ion exchange resin)
Halobacterium – 0.04 mM 6.0 9.3 Bader et al. (2018, 2017)
Streptomyces levoris 15 0.1 mM 3.5 9.04 Tsuruta (2004)
Bacillus sp. (dwc-2) 0.5 10 mg/L 3.0 3.03 Li et al. (2014)
Streptomyces sporoverrucosus dwc-3 100 0.042 mM 3.0 3.0 Li et al. (2016a,b)
of B. subtilis in alginate-chitosan microcapsules for uranium removal. These alginate-chitosan microcapsules had good
mechanical strength along with a high loading capacity of 374.64 mg U/g biomass. It was the first report on sequestration
of uranium by alginate-chitosan microcapsules. The immobilization of biomass will offer the feasibility of its application
in bioremediation technology.
Similarly, unicellular yeast and filamentous fungi were studied for biosorption of uranium (Table 3). Live cells, dead
cells and modified cells have been used to study the uranium biosorption capacity. Uranyl adsorption by magnetically
modified Rhodotorula glutinis was studied successfully (Bai et al., 2012). Magnetic adsorbents have the advantage of
the trouble-free separation of compounds from solutions. Rhodotorula glutinis cells were also immobilized in Ca-alginate
beads and investigated for uranium removal capacity (Bai et al., 2014). The typical regular lab strain ascomycetous yeast
Saccharomyces cerevisiae has also been reported for uranyl adsorption. Heat killed cells of Saccharomyces cerevisiae have
shown the higher biosorption capacity than the live cells (Lu et al., 2013; Wang et al., 2017). In a recent study by Han et al.
(2020) described the extreme uranium biosorption capacity by tri-amidoxime modified marine fungus material which was
prepared by condensation, nucleophilic substitution, electrophilic addition and then nitrile amidoxime. This functionalized
5
Table 3
Uranium biosorption capacities of different fungi.
(mg) (mg/g)
Schizophyllum commune 300 0.0021–0.5 mM 5.0–6.0 280 Günther et al. (2014)
Rhodotorulla glutinis (magnetically modified) 5.15 0.420 mM 6.0 235 Bai et al. (2012)
Trichoderma harzianum 0.420 4.20 mM 4.5 196 Akhtar et al. (2009)
Lentinus sajor- caju (Alkali treated) – 0.840 mM 4.5 182 Bayramoǧlu et al. (2006)
Acremonium minutisporum 40 100 mg/L 3.5 162.1 Gargarello et al. (2008)
Aphanocladium spectabilis 40 100 mg/L 3.5 161.5 Gargarello et al. (2008)
Rhodotorulla glutinis (raw) 4 0.588 mM 6.0 98.4 Bai et al. (2010)
Saccharomyces cerevisiae (heat killed) 25–200 1 mg/L 5.0 94.9–4.3 Wang et al. (2017)
Saccharomyces cerevisiae(PAO-B modified) 1 60 mg/L 6.0 47.4 Bai et al. (2016)
Saccharomyces cerevisiae (heat killed) – 0.0042 mM 5.5 29.8 Lu et al. (2013)
Rhodotorulla glutinis (immobilized) 5 0.153 mM 6.0 17.3 Bai et al. (2014)
Fusarium sp. #ZZF51 100 0.21 mM 4.0 16 Yang et al. (2012)
Saccharomyces cerevisiae (Live) 25–200 1 mg/L 5.0 3.2–1.9 Wang et al. (2017)
Table 4
Uranium biosorption capacities of different algae.
(mM) (mg/g)
Cystoseria indica (calcium pretreated) – 1.47 4.0 455 Khani et al. (2006)
Padina sp – 0.210–4.20 4.0 377 Khani (2011)
Catenella repens 50 mg 0.420 4.5 303 Bhat et al. (2008)
Cystoseria indica – 0.210–4.20 4.0 198 Khani et al. (2008)
Cladophora hutchinsiae 12 g/L 5.0 152 Bağda et al. (2017)
Chlorella vulgaris (dead) – 0.1 4.4 28 Vogel et al. (2010)
Chlorella vulgaris (live) – 0.1 4.4 14 Vogel et al. (2010)
Table 5
Uranium biosorption capacities different biosorbents of plant and animal origin.
Biosorbent Loading capacity Ref.
(mg/g)
Aloe vera waste (NaOH treated) 370.4 Noli et al. (2019)
Pollen pini 170.6 Carolin et al. (2017)
Grape stalks 115 Anagnostopoulos et al. (2015)
Human hair 62.5 Saini and Melo (2015)
Cactus fibres 62 Prodromou and Pashalidis (2013)
Eucalyptus citriodora distillation sludge 57.75 Bhatti and Hamid (2014)
Tea waste 29.41 Li et al. (2015)
Shrimp cells 25.77 Ahmed et al. (2014)
Sugar beet pulp 20.45 Nuhanović et al. (2019)
Date stones (PE and HCl treated) 19.6 Sirry et al. (2019)
Citrus lemon peels 5.7 Šabanović et al. (2019)
Rice stem (NaOH treated) 1.89 Xiao-Teng et al. (2019)
fungal material has the maximum loading capacity of 584.60 mg U/g contrary to raw mycelial of 15.46 mg U/g. Recently,
marine yeast Yarrowia lipolytica has been explored for uranyl removal (Kolhe et al., 2020). Y. lipolytica showed a biphasic
uranium binding pattern with a maximum loading capacity of 37.5 mg U/ g dry weight of cells. In filamentous fungi,
Trichoderma harzianum, Aphanocladium spectabilis, Lentinus sajor- caju, Schizophyllum commune and others were found to
be useful in uranium biosorption with significant efficiency (Table 3).
Algae are photosynthetic, eukaryotic aquatic organisms. Biosorption of uranium by different groups have also been
reported (Table 4). Cystoseira indica, a brown algae biomass was investigated for uranium biosorption. The maximum
loading capacity of Ca-pre-treated, protonated, and non-protonated Cystoseira indica was 454.5, 322.58 and 224.67 mg/g,
respectively (Khani et al., 2006). Padina sp., a marine brown algae biomass, was studied for removal of aqueous uranium
solution, and it could load up to 377 mg /g (Khani, 2011).
Several studies have been reported with a high biosorption capacity, selectivity, and still, there has always been a
demand for low-cost adsorbents. Recently much research has been focused on developing the eco-friendly and cost-
effective biosorbents. Among them a variety of plant and animal-derived biosorbents have been tested for uranium
biosorption. Table 5 represents some of the biosorbents studied for uranium biosorption from aqueous solutions.
Since biosorption is a physicochemical process, many factors influence the biosorption of uranium such as competing
ions, pH of the solution, amount of sorbent and contact time. Of all the factors, pH is the most critical factor because
of different speciation of uranium at different pH conditions (Table 6). For instance, in oxic conditions at pH ≤ 5
6
Table 6
Uranium speciation in different experimental media as predicted by Visual MINTEQ software.
Uranium concentration Conditions pH Dominant species Ref.
5 mM Ca & 2.5 mM Ca2 UO2 (CO3 )3 aq
87 µM Uranyl nitrate KHCO3 7.3 Carvajal et al. (2012)
0 Mm Ca & 2.5 mM UO2 (CO3 )2 2−
KHCO3
0 Mm Ca & 5 mM UO2 (CO3 )3 4−
KHCO3
LPM media (UO2 )2 CO3 (OH)3 −
0.5–1 mM Uranyl nitrate 7 Lopez-Fernandez et al. (2018)
NaClO4 (UO2 )4 (OH)7 + &
(UO2 )3 (OH)5+
5 mM G3P & 10 mM 6.8 (UO2 )2 (OH)5 + &
1 mM Uranyl carbonate Kulkarni et al. (2016)
MOPS (UO2 )4 (OH)7 +
5 mM G3P, 2.4 mM 9 UO2 (CO3 )3 4−
Ammonium Carbonate &
10 mM MOPS
1 mM Uranyl nitrate 100 mM Acetate buffer 5 UO2 2+ & UO2
Acetate+ Chandwadkar et al. (2018)
7 (UO2 )3 (OH)5 + &
1 mM Uranyl carbonate 20 mM MOPS Buffer
(UO2 )4 (OH)7 +
9 (UO2 )3 (OH)7 − ,
UO2 (CO3 )2 4−
& UO2 (CO3 )3 4−
03–05 UO2 2+ ,
100 mg/L U as Uranyl nitrate 14.56 mM Na2 CO3 Huang et al. (2017)
(UO2 )2 (OH)2 7+
& UO2 CO3
05–08 UO2 (CO3 )2 2− &
UO2 (CO3 )3 4− O2 (CO3 )3 4−
free uranyl ion (UO22+ ) is the dominant species, (UO2 )3 (OH)5 + at pH 5.5–6.0, from pH 6.0–7.5 the mixed uranyl-
hydroxide-carbonate species, UO2 (OH)3 CO3 − and UO2 (CO3 )2 2− is the dominant uranyl species at pH >7.5. The above
U speciations are at environmentally relevant conditions and increase in U concentration cause a shift in the percentage
distribution of U (Konstantinou and Pashalidis, 2004). The concentration of metal and pH are the two crucial factors that
influence speciation. At different pH and uranium concentrations, uranyl ion is present in various forms like UO2 OH+ ,
UO2 (OH)2 (aq),(UO2 )2 (OH)2 2+ , (UO2 )3 (OH)5 + , (UO2 )4 (OH)7 + , (UO2 )3 (OH)7 − and UO2 (OH)3 . At alkaline pH and when the
carbonate concentration increases, mono-, di- and tri-nuclear uranyl carbonate species, UO2 CO3 (aq), UO2 (CO3 )2 2− and
UO2 (CO3 )3 4− are dominant (Acharya, 2015). Thus, increased biosorption was observed at lower pH values. The decreased
biosorption of uranium at alkaline pH was due to the mutual repulsion of negatively charged uranyl carbonate species
and negatively charged biosorbents (Song et al., 2019).
There have been numerous studies that are being published every year on biosorption based remediation. Biosorption
based treatment processes are low cost, highly efficient and biosorbent, and metal recovery is also possible. However,
commercially applied biosorption techniques are rare. Primarily, research in this area is focused on choosing the different
biosorbent, its characterization and studying the different parameters like biomass dosage, initial metal concentration,
the effect of pH and competing ions. Besides, in laboratory experiments were conducted in a very controlled manner.
Whereas in natural environments, conditions would be different and dynamic. For a technique to make it available at
an industrial scale, more studies on pilot projects are required. Another major limitation in uranium biosorption is pH.
There is significantly less information available on the uranium biosorption at alkaline pH and much attention to be given
in this area of interest. Moreover, the waste generated in the mining or nuclear industry could have other radionuclides
and heavy metals. Hence, future works should be focused on biosorbents with high adsorption capacity, selectivity and
radiolytic stability along with surface functionalization.
3.2. Biomineralization
Biomineralization or bioprecipitation is the formation of insoluble uranium precipitate by complexation with the
inorganic ligands such as phosphates, through an enzymatic process (Renninger et al., 2004). The microbial phosphatase
enzymes hydrolyse the organic phosphate substrate and release the inorganic phosphate, which forms a metal-phosphate
insoluble precipitate (Zhao et al., 2019). Generally, three types of mechanisms have been reported for uranium biominer-
alization: (1) metabolism induced biomineralization, (2) extracellular precipitation and (3) precipitation at cell surface
due to nucleation of phosphate minerals (Jiang et al., 2020). Fig. 2 represents the general mechanism of uranium
biomineralization.
Several reports have been published in this field for remediation of heavy metals and radionuclides. For instance,
Bacillus and Rahnella spp. were tested positive for phosphatase activity and precipitated 73% and 95% of U from 200
7
Fig. 2. Schematic representation of biomineralization of uranium.
µM uranyl acetate and 10 mM glycerol-3-phosphate, respectively. A negative phosphatase Arthrobactor sp. isolated
from subsurface soils at the US DOE Oak Ridge Field Research Center (ORFRC) did not precipitate the uranium (Beazley
et al., 2007). Shewanella putrefaciens immobilized uranium as chernikovite [H2 -(UO2 )2 (PO4 )2 .8H2 O], on the cell surface
at slightly acidic pH (Huang et al., 2017). At neutral pH, Aeromonas hydrophila, Pantoea agglomerans, and Pseudomonas
rhodesiae strains have mineralized the uranium as insoluble hydroxyapatite [Ca5 (PO4 )3 OH] in aerobic and nitrate-reducing
conditions (Shelobolina et al., 2009). Indigenous bacteria present in uranium mine waters at Uranium Corporation of India
Limited (UCIL), revealed an exceptional uranium biomineralization property. This strain could remove 99% of soluble
U(VI) as crystalline uranyl phosphate species [(UO2 (PO3 )2 , (UO2 )3 (PO4 )2 H2 O, and UO2 (PO4 )2 ] (Choudhary and Sar, 2011).
Biomineralization by phytate was also demonstrated in uranium-contaminated sediments of ORFRC (USA). Hydrolysis
of phytate releases the inorganic phosphate which precipitates uranium as ternary sorption complexes, U(VI)-phytate
precipitate and U(VI)-phosphate mineral. In a study by Beazley et al. (2011), nearly complete phytate hydrolysis was
noticed at pH 5.5. Bioprecipitation of uranium by isolates Bacillus sphaericus JG-7B and Sphingomonas sp. S15-S1 at acidic
conditions via acid phosphatase was also reported (Merroun et al., 2011). Initial sorption followed by biomineralization
was reported using B.cereus 12–2 sp. and suggested that the extracellular amorphous U containing particles were
transferred into the cell and converted into uramphite intracellularly by phosphatase (Zhang et al., 2018). High efficient
biomineralization of uranium by Stenotrophomonas strain Br8 cells was observed by Sánchez-Castro et al. (2020). Br8 cells
were able to immobilize up to 373 mg U/g bacterial dry weight through high phosphates activity. The needle-like fibrils
precipitated at the cell surface and in the extracellular space were identified as meta-autunite. Staphylococcus aureus
biofilms have also been studied recently for uranium sequestration in which, the acid phosphatase activity of biofilms
presented a new method for bioremediation (Shukla et al., 2019). Yiqian Wang et al. (2019) studied the synergetic
biosorption and biomineralization of uranium by Kocuria sp. The observations revealed that the first fast adsorption
of uranium on cell surface followed by gradual precipitation. This study also highlighted the role of phosphates in
biomineralization of uranium. The phosphatase enzymes responsible for the activity were identified as PhoY and phytase
in Caulobacter crescentus (Yung and Jiao, 2014), PhoK (alkaline phosphatase) in Sphingomonas sp. BSAR-1 (Nilgiriwala et al.,
2008) and PhoN (acid phosphatase) in Serratia sp. (Paterson-Beedle et al., 2012).
Several recombinant strains such as E. coli with acid phosphatase genes (Basnakova et al., 1998), P. veronii and P.
rhodesiae with alkaline phosphatase genes (Powers et al., 2002), and D. Radiodurans (Appukuttan et al., 2006) were
developed for biomineralization of uranium. Recombinant E. coli DH5α bearing cloned phoN was able to sequester uranyl
ion (UO2 2+ ) from dilute aqueous flows as polycrystalline uranyl phosphate (HUO2 PO4 ). Genetically modified strains of
P. veronii and P. rhodesiae with alkaline phosphatase genes (phoA) accumulated sufficient PO4 3− which allowed the
precipitation of uranium. D. radiodurans was engineered with phoK gene from Sphingomonas sp. which encodes novel
alkaline phosphatase. This Deino-PhoK recombinant strain can precipitate >90% of uranium from 1 mM solution at pH
9.0. The precipitated uranyl phosphate complex was identified as chernikovite. Another recombinant D. radiodurans strain
with phoN from Salmonella enteric serovar Typhi, codes for non-specific acid phosphatase, retained the bioprecipitation
ability even after 6 kGy of 60 Co gamma irradiation.
In addition to bacteria, fungi are also reported to mineralize the uranium (Gadd and Fomina, 2011). Several yeast strains
have also been studied for phosphatase mediated uranium biomineralization and reported that initial sorption of uranium
to the cell surface and subsequent precipitation (Lopez-Fernandez et al., 2018). In yeast strains, Cryptococcus filicatus,
Kluyveromyces lactis, and Pichia acaciae phosphatase mediated uranium precipitation was reported when augmented
with glycerol-2-phosphate (G2P). This U-phosphate bio-mineral complex was identified as ankoleite, chernikovite,
bassetite, and uramphite by XRD analysis (Liang et al., 2016). Biomineralization of uranium was reported via uranyl
8
phosphate formation in Saccharomyces cerevisiae when grown in high phosphate containing media (Öhnuki et al., 2005).
In filamentous fungi, Aspergillus niger and Paecilomyces javanicus uranium biomineralization was observed when organic
phosphorous G2P was supplied externally. The formed bio-minerals were identified as potassium uranyl phosphate
hydrate, meta-ankoleite, uranyl phosphate hydrate, meta-ankoleite, uramphite, and chernikovite (Liang et al., 2015).
Microorganisms were reported to precipitate uranium depending on speciation in environmental conditions (Kulkarni
et al., 2016; Neiss et al., 2007). Speciation ultimately depends on the pH of the environment. In oversaturated conditions,
uranium precipitates with calcite, whereas in under-saturated condition uranyl complexes with calcium or carbonate,
thereby increasing its mobility (Catalano et al., 2006). In a natural environment where calcium and carbonates are
relatively high and at alkaline pH uranium is present as Ca2 UO2 (CO3 )3 and UO2 (CO3 )3 4− which further increases the
mobility (Bernhard et al., 2001; Zheng et al., 2003). Besides, the activity of phosphatase enzyme, the surface of microbes
has also influenced by the pH (Beazley et al., 2011; Gavrilescu et al., 2009). Tu et al. (2019a) attempted to study the impact
of humic substances (HA) and fulvic acid (FA) on uranium biomineralization by Bacillus sp. dw-3. The results suggested
that the HA and FA did not affect the biomineralization process. Tu et al. (2019b) also investigated the influence of organic
ligands such as acetate, lactate, salicylate, and citrate to oxalate on uranium biomineralization. The results indicated that
strong acids like oxalate and citrate affected the biomineralization process. Recently, simultaneous removal of nitrate and
uranium was achieved by Vijay et al. (2020) in microbial fuel cells (MFC). Nitrate exists as co-contaminant in uranium-
contaminated sites, and it also enhances the reoxidation of reduced uranium. The denitrifying bacteria consortia at MFC
cathode produced phosphatase enzyme which precipitated the soluble uranium into uranyl phosphate with a power
density of 2.91 Wm−3 and nitrate removal rate of 0.130 kg NO3 − -N m−3 d−1 .
Microbial induced biomineralization is gaining importance as a new technique in the field of uranium bioremediation.
However, the major problem associated with biomineralization as a remediation strategy is its economic viability. The
usage of organic phosphate as a donor may limit its application as in situ radionuclide remediation technique. Another
problem with this technique is the precipitation of metal on the surface of the cell may hinder the metabolism of the
organism and may lead to reduced efficiency (Dummi Mahadevan and Zhao, 2017). Hence, a primary concern should be
given in identifying microbial strains with high phosphate activity, tolerance to toxic metals and extreme pH conditions
(Jiang et al., 2020). Further, research to be focused on long term effective on-site remediation strategies.
3.3. Bioreduction
Reduction process of U(VI) to U(IV), makes insoluble precipitate of uranium and sequester it from groundwater.
Uranium reducing microorganisms are ubiquitous, and it was first demonstrated in Micrococcus lactilyticus (Woolfolk and
Whiteley, 1962). More than 25 species of prokaryotes have been identified which are involved in uranium reduction. For
example, iron-reducing bacteria (Geobacter uraniireducens and Geobacter daltonii) and sulphate-reducing bacteria (SRB)
(Desulfovibrio, Desulfobacterium, and Desulfotomaculum genera) could able to reduce U(VI) to U(IV) (Akob et al., 2012).
These bacteria can use uranium as an electron donor in addition to iron and sulphate. Other uranium reducing bacteria
are Clostridium sp. (Gao and Francis, 2008), Thermus scotoductus SA-01 (Cason et al., 2012), Anaeromyxobacter dehalogenans
strain 2CP-C (Wu et al., 2006), and facultatively anaerobic Bacillus sp dwc-2 (Li et al., 2017a,b). The pilot-scale and in situ
studies have demonstrated that the reduction is the only viable option for large contaminated sites (Lakaniemi et al., 2019).
For instance, in the long term (∼2 years) experiment at contaminated sites (up to 60 mg/L and 800 mg/kg solids) of the
US Department of Energy at Oak Ridge, the augmentation with external organic acids has facilitated the bioreduction of
uranium (Istok et al., 2004).
Pathway of uranium reduction, enzymes, or genes responsible and the number of electrons involved has not been well
established yet. Generally, the reduction of U(VI) to U(IV) needs two electrons. Though, literature reports suggest a single
electron reduction system is the most likely mechanism of reduction. One electron reduction mechanism was explained
by using G. sulfurreducens in which U(VI) initially reduced to U(V) by one electron and then to U(IV) by disproportionation
(Lloyd and Renshaw, 2005). The mechanisms and enzymes involved in the uranium reduction are different for different
organisms. Crude cell extracts, whole-cell experiments and mutational analysis of D. vulgaris have suggested the role of
cytochrome c3 in U(IV) reduction (Lovley et al., 1993). It has been reported that bacterial pili act as electron conductors
between cells and an electron acceptor (Reguera et al., 2005). Microscopic studies revealed that the reduced U (IV) was
predominantly localized at periplasm and outside of the cells. It indicates that outer membrane-bound enzymes are
responsible for uranium reduction (Majumder and Wall, 2017). Fig. 3 describes the general aspects of the bioreduction
process.
Bioreduction seems to be a more attractive choice when compared to other alternatives such as biosorption or
bioaccumulation for in situ bioremediation of uranium contaminated sites. The reduction of U(VI) to U(IV) leads to effective
containment. Pilot-scale studies have demonstrated the successful in situ bioreduction of uranium. For example, in a study
at Oak ridge, U.S., when the groundwater and subsurface were supplemented with electron donors, bioreduction was
achieved to a sub-micromolar level. It has been observed that conditioning with electron donors stimulated the growth
of denitrifying, iron-reducing, and sulphate-reducing bacteria (Istok et al., 2004). When sites were enriched with slow-
release substrates such as emulsified vegetable oil, U(VI) reduction was noticed with Comamonadaceae, Geobacteriaceae
and Desulfobacterales (Gihring et al., 2011). Similarly, in a recent study, uranium reduction was observed in iron oxide-rich
sediments after ethanol supplementation (Li et al., 2018).
9
Fig. 3. Schematic representation of bioreduction of uranium.
Whilst in situ studies have shown bioreduction as a practical approach; it also encompasses some significant challenges.
The major problem associated with the in situ uranium bioreduction is the stability of reduced U(IV). Studies had shown
that when biogenic uraninite was exposed to oxygen, it readily reoxidized to U(VI), making it a futile bioremediation
strategy. Similarly, nitrate, manganese oxides, and iron oxides also facilitated the reoxidation of uranium (Abdelouas et al.,
2000; Finneran et al., 2002; Fredrickson et al., 2002; Istok et al., 2004). Augmentation of contaminating sites with organic
compounds may stimulate the growth of non-target microbes (Anderson et al., 2003; Gu et al., 2005). Also, the presence
of organic ligands impairs the movement of the uranium, even in its reduced form. Clostridium sp. reduced the citric acid
associated with U(VI) as U(IV)-citric acid complex, which remained in solution instead of precipitation. It increases the
mobility in the environment and is a potential for contaminating groundwater and other sites (Francis and Dodge, 2008).
In the case of humic substances, it did not cause precipitation of reduced uranium. Instead, it remained in the solution as
U(VI)-humic complex (Gu et al., 2005; Wan et al., 2011).
Moreover, the end products formed also are essential factors to be considered during the uranium bioreduction process.
It has been reported that several U(IV) reduced products are being formed like biogenic uraninite, monomeric U(IV). It
is a well-known fact that the biogenic uraninites are more stable to reoxidation and preferred for bioremediation rather
than other forms (Bargar et al., 2008; Khijniak et al., 2005; Lee et al., 2010; Renshaw et al., 2005). However, studies have
also demonstrated the formation of amorphous mononuclear U(IV) and soluble organic ligand-bound U(IV), which are
less stable and extremely mobile.
Many environmental factors influence the in situ bioreduction processes, such as microbial community populations,
redox potential, pH, organic substrates, and presence of other contaminants. In this context, different bacterial community
predominates in different environmental conditions. In anaerobic uranium reduction, Geobacter spp. are dominant.
Similarly, Desulfovibrio spp. are prevailing bacteria in a sulphate-reducing enrichment and Clostridium spp., Ferribacterium
spp., and Geothrix spp. are mainly present in an iron-reducing environment (Boonchayaanant et al., 2009; Cardenas et al.,
2008). Elevated pH and presence of calcium or carbonates will decrease the uranium reduction process by forming the
calcium-uranyl-carbonate and uranyl-carbonate complexes, respectively. These uranyl complexes are highly soluble and
likely to decrease reduction (Brooks et al., 2003; Fox et al., 2013). Uranium bioreduction will be facile at pH 5.0 to 6.0 and
in the absence of ligands such as carbonates, phosphates, and sulphates. Uranyl hydroxyl complexes are readily reduced,
which are the dominant species in that condition. At different environmental pH conditions, quality and quantity of
microbial populations will also change. At neutral, pH Ralstonia and Dechloromonas spp., and an acidic pH Castellaniella and
Burkholderia spp. are widely studied (Spain and Krumholz, 2012). Presence of oxygen will affect the stability of reduced
uranium. Reports suggest that nearly all the bioreduced uranium is reoxidized over a while (Komlos et al., 2008). Nitrates
may also inhibit the uranium reduction process because of its higher electric potential (Istok et al., 2004). On the other
hand presence of sulphates increased the U(VI) reduction rates by both D. desulfuricans and a D. vulgaris and Clostridium
sp. coculture (Spear et al., 2000). Some electron donors such as acetate, glucose, lactate, ethanol and methanol, aromatic
hydrocarbons like toluene, pyruvate, fumarate, and emulsified vegetable oils have been tested for bioreduction and each
of which has its ability (Cardenas et al., 2008; Gihring et al., 2011; Luo et al., 2007; Madden et al., 2009).
3.4. Bioaccumulation
Bioaccumulation is the intracellular accumulation of sorbate. It is an energy-consuming process by which uranium

is sequestered by transporting inside the cell. Bioaccumulation mechanism can be divided into two stages: first quick
biosorption on the surface and next transport of sorbed metal inside the cell (Gerber et al., 2016) (Fig. 4). Uranium
has no biological function, and there are no transporter proteins identified yet for its transport into the cell. However,
uranium may accumulate inside of the cell due to increased permeability of the cell membrane when it is under heavy
metal or other stress condition. It is depicted that intracellular sequestration of uranium with the polyphosphates is a
detoxification mechanism (Suzuki and Banfield, 2019). For example, Arthrobacter ilicis accumulated uranium intracellularly
10
Fig. 4. Schematic representation of bioaccumulation of uranium.
as precipitates closely associated with the polyphosphate granules (Suzuki and Banfield, 2004). In another study by
VanEngelen et al. (2010) also reported the intracellular sequestration of uranium by internal phosphates as uranyl
phosphate. Bioaccumulation of uranium with polyphosphates has previously been studied in A. ferroxidans (Merroun et al.,
2003), and P. migulae CIP 105470 (Merroun and Selenska-Pobell, 2008).
Besides polyphosphate associated sequestration, needle-like fibrils formations have also been observed in the cy-
toplasm (Merroun et al., 2006). Similarly, Li et al. (2016a) have also observed that the uranium was accumulated
as needle-like granules on the cell wall and within the cytoplasm. Yeasts also had shown as efficient organisms in
bioaccumulation. In a recent study, Gerber et al. (2018) reported the active bioaccumulation of uranium by Rhodosporidium
toruloides in which intracellular uranium was detected as phosphorous-containing needle-like structures. Like in other
sequestration mechanisms, bioaccumulation was also influenced by pH, temperature, metal concentration and presence
of other contaminants. Moreover, there is no definite evidence available in open literature signifying bioaccumulation of
uranium could be a proper strategy for bioremediation of contaminated soil or water (Dummi Mahadevan and Zhao, 2017).
4. Conclusion
Bioremediation is gaining more importance to treat heavy metals contaminant sites due to its cost-effective, eco-
friendly, and superior efficiency over conventional methods. Various methods such as biosorption, bioreduction and
bioprecipitation have been tested by using a different group of organisms. Many of such strains have shown the ability
to minimize the bioavailability of the pollutant under laboratory studies. Nevertheless, in terms of significant scale
field application, none of them has proved to be efficient over a long time. Since the experimental conditions in the
laboratory are more convenient for the bacteria/algae/fungi than the actual environmental conditions. To overcome this
limitation, the specific metabolic activity of an organism and the environmental conditions must be studied. Hence, more
studies must be focused on the field application and fine-tuning the required parameters for better sustainability and
pollution-free environment.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have
appeared to influence the work reported in this paper.
Acknowledgement
The authors thank Dr B. Venkatraman, Director SQ&RMG, IGCAR for support and encouragement during this study.
This work was funded by Department of Atomic Energy, Government of India.
11
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Environmental Technology & Innovation

Microbial interactions with uranium: Towards an effective

2. Chemical methods for uranium sequestration

3. Microbial interactions with uranium

Fig. 1. Schematic representation of biosorption of uranium.

Fig. 2. Schematic representation of biomineralization of uranium.

Fig. 3. Schematic representation of bioreduction of uranium.

Bioaccumulation is the intracellular accumulation of sorbate. It is an energy-consuming process by which uranium

Fig. 4. Schematic representation of bioaccumulation of uranium.

Declaration of competing interest

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