Journal of Environmental Radioactivity 180 (2017) 27e35

Contents lists available at ScienceDirect

Journal of Environmental Radioactivity

journal homepage: www.elsevier.com/locate/jenvrad

Radiation, radionuclides and bacteria: An in-perspective review

Arpit Shukla, Paritosh Parmar, Meenu Saraf*
Department of Microbiology, University School of Sciences, Gujarat University, Ahmedabad 380009, Gujarat, India

a r t i c l e i n f o a b s t r a c t

Article history: There has been a significant surge in consumption of radionuclides for various academic and commercial
Received 22 June 2017 purposes. Correspondingly, there has been a considerable amount of generation of radioactive waste.
Received in revised form Bacteria and archaea, being earliest inhabitants on earth serve as model microorganisms on earth. These
18 September 2017
microbes have consistently proven their mettle by surviving extreme environments, even extreme
Accepted 19 September 2017
ionizing radiations. Their ability to accept and undergo stable genetic mutations have led to development
of recombinant mutants that are been exploited for remediation of various pollutants such as; heavy
metals, hydrocarbons and even radioactive waste (radwaste). Thus, microbes have repeatedly presented
Keywords:
Radionuclide
themselves to be prime candidates suitable for remediation of radwaste. It is interesting to study the
Radiation behind-the-scenes interactions these microbes possess when observed in presence of radionuclides. The
Bacterial interactions emphasis is on the indigenous bacteria isolated from radionuclide containing environments as well as the
Bioremediation five fundamental interaction mechanisms that have been studied extensively, namely; bioaccumulation,
Biotechnology biotransformation, biosorption, biosolubilisation and bioprecipitation. Application of microbes exhibiting
Bacteriology such mechanisms in remediation of radioactive waste depends largely on the individual capability of the
species. Challenges pertaining to its potential bioremediation activity is also been briefly discussed. This
review provides an insight into the various mechanisms bacteria uses to tolerate, survive and carry out
processes that could potentially lead the eco-friendly approach for removal of radionuclides.
© 2017 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28
2. Radiation and microorganisms: exposure and survival . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28
2.1. Effect of ionizing radiations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28
2.2. Mechanism of resistance and/or tolerance to ioning radiations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28
3. Soil and microorganisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28
3.1. Soil as habitat . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28
3.2. Radionuclides in soil . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28
3.3. Interactions between bacteria and radionuclides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29
3.3.1. Bioaccumulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29
3.3.2. Biosorption . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30
3.3.3. Biotransformation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31
3.3.4. Biosolubilisation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31
3.3.5. Bioprecipitation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31
3.3.6. Miscellaneous . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31
4. Microbial remediation of radionuclides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32
5. Challenges and future prospects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34

* Corresponding author.
E-mail addresses: [email protected] (A. Shukla), [email protected]
(M. Saraf).

https://doi.org/10.1016/j.jenvrad.2017.09.013
0265-931X/© 2017 Elsevier Ltd. All rights reserved.
28 A. Shukla et al. / Journal of Environmental Radioactivity 180 (2017) 27e35

1. Introduction were found to limit the toxic effects of U. (Choudhary et al., 2012;
Merroun and Selenska-Pobell, 2008; Choudhary and Sar, 2011;
Microorganisms, being the witness and survivor of various Suzuki and Banfield, 2004). Bioadsorption and ‘localized biomin-
extreme conditions on Earth over the time, are today been eralization’ have shown to be responsible for providing uranium
exploited in remediation of radioactive waste. They possess the resistance to Pseudomonas aeruginosa J007 and Arthrobacter nic-
advantage of being environment friendly, easy to grow, adapt- otianae (Suzuki and Banfield, 2004). It was recently discovered a
ability, specificity, ability to carry out desirable reactions and unique interaction between bacteria, isolated from spent nuclear
processes-with generation of no or minimal polluting byproducts. fuel pond, and Co2þ. It showed that the tolerance to cobalt was due
They possess the characteristic self-sustaining capability (Gazso
, to an efficient efflux pump mechanism similar to that of Ni2þ and
2001). This review provides an insight into the occurrence of mi- Zn2þ -since cobalt tolerance is usually associated with them
crobes in environments containing radionuclides, the mechanisms (Dekker et al., 2014). Members of genera Serratia are known to be
involved for its survival and tolerance to radiation with special resistant to Cs137, Sr90 and Co60 (Paterson-Beedle et al., 2006).
emphasis on the interactions between the bacterial cell and ra- Resistance to nickel and cobalt in E. coli has been acknowledged to
dionuclides which show immense potential for bioremediation. the presence of a novel YohM protein rcnA, a first that does not rely
The use of bacteria in bioremediation of radionuclides is also briefly on the traditional NiCoT (Nickel Cobal Transporter) family
discussed later in this review. (Rodrigue et al., 2005). S-layer proteins have also been identified to
provide resistance against gamma-radiation (Gerbino et al., 2015).
2. Radiation and microorganisms: exposure and survival The studies following the devastating accident in Chernobyl
revealed that radiation from nuclear power plant had a positive
2.1. Effect of ionizing radiations effect on in spore germination in areas, affected by radiation. The
phenomena was later termed as ‘radiostimulation’ (Dadachova and
It is important to acknowledge the lethal implications of Casadevall, 2008). In the same study, Chernobyl-associated fungi
radioactive substances. Gamma rays and other ionizing radiations, exhibited radiotropism and exhibited their ability to utilize radia-
in general, have been known to inhibit reproduction of microbes by tion as source of energy.
engaging in alteration of DNA (IAEA, 2017). The detrimental effects
of ionizing radiations occur on the core nuclear material of any cell-
3. Soil and microorganisms
the DNA. Exposure to such stress could lead to formation of lesions
leading degradation of DNA by direct and indirect mechanisms.
3.1. Soil as habitat
Directly, an electron is ejected out of the DNA whereas indirect
pathway involved the process of radiolysis (Ravanat and Douki,
Soil serves as one of the most important habitats. Teeming with
2016).
variety of nutrients, organic matter and even metals soil serves as
one of the most economical ecosystems for the growth and pro-
2.2. Mechanism of resistance and/or tolerance to ioning radiations
liferation of microbes. From species (taxonomic) to functional and
from proteomic to genomic, soil continues to swell the already
The most radioresistant bacteria, Deinococcus radiodurans has
exhausting list of microbes. As previously mentioned, microbes
been studied extensively. Lethal dose (LD10) for D. radiodurans R1
have even been isolated from soils containing radionuclides.
has been calculated to be 10
103 Sv (Hitoshi et al., 1983). Few
species of Deinococcus and Rubrobacter have been identified to
survive gamma radiation doses of greater than 25
103 Sv. Some 3.2. Radionuclides in soil
species of Chroococcidiopsis have been reported to survive up to
15
103 Sv and with members of genus Micrococcus exhibiting a Radionuclides are usually been dispersed in nature, in minute
more humble radiation resistance (Brim et al., 2000; Krabbenhoft concentrations. Natural radioactivity results primarily due to 4 K
et al., 1965). Radionuclide 241Am imparted a chronic effect on the and from the members of 238U decay chain. Incidence of U, Rn, Th in
growth of Photobacterium phosphoreum, a bioluminescent bacte- agricultural lands of Bulgaria and Cu, Cd and Pb from acid drainage
rium, with a decrease in its growth while increasing the intensity waters have instigated the development of various bioremediation
and duration of its luminescence at low temperatures. Alexandrova techniques for radionuclide pollutants (Groudev et al., 2001).
et al. (2011) attributed it to the formation of peroxides in the me- Following the applications of Rhodococcus, Nocardia and Dein-
dium solution resulting from radiolysis of water. The same study ococcus radiodurans in remediation of radwaste with concentra-
also noted the accumulation of 241Am in DNA of the bacterium. In tions greater than 10 mCi of 137Csg1 and for concentrations greater
addition to radiation, the bacteria have also exhibited resistance to than 20 mCi 137Csg1 respectively, model microbes Deinococcus
desiccation, ultraviolet radiation and oxidative agents. While radiodurans, Pseudomonas putida, Shewanella putrefaciens CN32
investigating the cause of such immense resistance, the presence of have been reported to be used as pure culture in remediation (Lloyd
multiple pathways for amino acid synthesis have been identified and Renshaw, 2005). Commercial acid-leaching of radionuclides
(Venkateswaran et al., 2000). It was found that accumulation of Mn from mine has been one of the prime causes of terrestrial presence
(II) in the bacterium promoted resistance (Daly et al., 2004). The of radionuclides (U, Th, Pu) and some heavy metals (Cu, Cd, Pb) in
genetic basis for radiation resistance in the bacterium was found to agricultural lands in Bulgaria (Groudev et al., 2001). A recent study
be an exonuclease repair pathway, as investigated by Misra et al. devised an expedient method for identification and estimation of
(2006). Deinococcus radiodurans was been found to survive concentration of naturally occurring radioactive material (NORM)
ionizing radiation levels up to 10
103 Sv (Cox and Battista, 2005). in soil horizons (Michalik, 2017). It has been duly emphasized upon
U, Ni, Co, Cu and Cd resistant bacteria belonging to the genus Ba- that, chronic radiation in an oligotrophic environment leads to
cillus, Serratia and Arthrobacter, Pseudomonas, Rhodococcus, Bacillus excersion of selective pressure to enhance certain microbes which
were been discovered. Upon subjected to further studies, resistance significantly alters the richness, diversity and abundance of bacteria
was revealed to be due to instrinsic characteristics of the bacteria. in that environment (Tisa
kova
et al., 2013). In India, naturally
Intracellular sequestration of U was found to contribute to resis- occurring radionuclides are; 238U, 232Th, 4 K, 226Ra, Ca. Levels of
tance while processes such bioprecipitation and biomineralization radiation in South Konkan village soil are 68.08
109 Svh1.
 A. Shukla et al. / Journal of Environmental Radioactivity 180 (2017) 27e35 29

Responsible radionuclides are 238U, 232Th, 4 K (Dhawal et al., 2013). various factors affecting interactions between microbes and ra-
In the South Indian coastal state of Karnataka radionuclides 232Th, dionuclides in soil had been carried out and stated in the 5th Eu-
4
K, 226Ra account for 74
109 Svh1 (Narayana et al., 2001). ropean Framework Program: BORIS. It primarily focused on the
Presence of 238U, 232Th, 4 K in another coastal South Indian state of bioavailability of Cs, Sr and Tc in soil (Tamponnet et al., 2008).
Tamil Nadu has also been described (Ravisankar et al., 2012). In the Often, the mechanisms involved in interaction between radionu-
western state of Gujarat, occurrence of radioisotopes of Th and Ca clide and microbe also include metals (Tabak et al., 2005; Van
from Naredi Cliff and, U and Th in the groundwater of Thar Desert Hullebusch et al., 2005). Uranium, one of the most crucial radio-
respectively, has been reported (Sahay et al., 2015). In the north- nuclides with wide applications, exists in soil in the oxidation states
eastern Indian state of Jharkhand, uranium mining and milling of U(IV) and U(VI). Both are soluble in water and their migration is
from Jaduguda uranium mine into the Bay of Bengal have been heavily dependent on pH, ligand concentrations and redox status
found to be emitting alpha particles that has affected the local (Krupka et al., 1999). A list of indigenous bacteria isolated from
microbial communities (Dhal and Sar, 2014). radioactive sample is presented in Table 1.
Microbial biomass had been known to possess a relatively
greater affinity towards U, Cs and Pu. This reassures their applica-
3.3. Interactions between bacteria and radionuclides tion in removal of radionuclides from environment (Tisa
kova

et al.,
2013). Bacteria interact with radionuclides in various ways, as
It is due to the presence of soil-dwelling microbes that the enlisted in Table 2. It is interesting to note that, the actual mecha-
biogeochemical cycling of N, C, S, P and Fe occur (Prescott et al., nisms of interaction of bacteria with radionuclides is in many ways
2006). Nevertheless, before commencing the process of biogeo- similar to those of heavy metals. Various sub-interactions have also
chemical cycling of compounds, microbes must first interact with been listed in the table however, they work on the fundamental
them. Such processes take place only after successful interactions principles of biotransformation, biosorption, bioaccumulation,
between the microbial cell and the nuclide. To study such in- bioprecipitation and biosolubilisation. These five principles are
teractions, a remarkable notion of bioavailability and bio- described in detail.
accessibility has to be recognized. It is represented by solid-liquid
distribution coefficient (Kd) and it acts as growth limiting factor for
any ecosystem. Kd signifies the ratio of concentration of radionu- 3.3.1. Bioaccumulation
clide activity adsorbed by a solid phase to the concentration of Bioaccumulation is the “retention and concentration of a sub-
radionuclides absorbed in the aqueous phase, as Bq kg1 soil stance within an organism” (Tabak et al., 2005). Jorgensen (2010)
(Tamponnet et al., 2008; Sheppard et al., 2009). For this review, it is summarized bioaccumulation as “an enrichment of contaminants
imperative to consider the role of bioavailability of radionuclides in in organisms relative to that environment.” The phenomena of bio-
soil. Haferburg and Kothe (2007), discussed presence of noxious concentration and biomagnification comprise bioaccumulation. It
contaminants in biotopes. They attributed bioavailability to be relies on adsorption of radionuclides on to the cell surface due to
reliant on the constitution of soil matrix, climatic conditions, mi- electrostatic attraction forces existing between the metal cations
crobial activity and water flow. Fig. 1 summarizes various mecha- and the negatively charged cell surface, resulting in an electrostatic
nisms of interactions found in bacteria. In soil, radionuclide cations binding. Staunton et al. (2002) found a decrease in distribution
are less mobile (Shaowei et al., 2017). A detailed investigation of coefficient of radiocaesium with an increase in organic matter in

Fig. 1. Various interaction mechanisms between microorganisms and radionuclides.

30 A. Shukla et al. / Journal of Environmental Radioactivity 180 (2017) 27e35

Table 1
Various indigenous bacteria isolated from radioactive sample.

Sample Bacteria present Reference

Cs137 Rhodococcus, Nocardia Lloyd and Renshaw, 2005

Tc99 Deinococcus radiodurans Lloyd and Renshaw, 2005
Pu
Midnite mine Bacillus cereus, B. pumilis, Arthrobacter ilicis, A. ramosus, R. globerulus Suzuki and Banfield, 2004
Uranium ore, U-contaminated waste Pseudomonas, Stenotrophomonas, Actinobacter, Enterobacter, Microbacterium Islam and Sar, 2011;
Choudhary and Sar, 2011b
U mill tailing soil sample containing 238U, 235U, 4 K, Acidobacteria, Actinobacteria, Serratia sp., Hafnia sp., several uncultured bacteria Yan and Luo, 2015
226
Ra and 232Th
Mashhad soil sample Micrococcus lylae Misra et al., 2006
Oil waste containing hydrocarbons and radionuclides Burkholderia, Bradyrhizobium jicamae, Hydrogenobacter hydrogenophilus Gerbino et al., 2015
222
Rn, 228Ra and 226Ra containing groundwater Bacillus, sp., Methylobacterium sp., Enhydrobacter sp., Erythrobacter sp., Brim et al., 2000;
Sphingomonas sp., Kocuria, Pseudomonas grimontii, Mycobacterium hodleri Luk'yanova et al., 2008
Soil R. erythropolis, Rhodococcus sp., P. fluorescens Tamponnet et al., 2008
Spent nuclear fuel pool (SNFP) water Kocuria palustris, Pseudomonas aeruginosa, Micrococcus luteus, Ochrobactrum Tisa

kova

et al., 2013
spp.
Uranium ore deposit Arthrobacter, Microbacterium, Acinetobacter, Stenotrophomonas Islam and Sar, 2011
Nuclear fuel storage pond Cupriavidus metallidurans, Curvibacter, Tardiphaga, Serratia, Yersinia Brim et al., 2000

Table 2
Mechanisms of interaction between microbes and radionuclides.

Mechanism of interaction Source

Bioaccumulation Haferburg and Kothe, 2007

Biosorption
Bioprecipitation
Extracellular sequestration
Transport mechanisms  ATP-binding cassette transporters
 Efflux transporters
Biooxidation Rui et al., 2013
Biosolubilisation
Adsorption Yin et al., 2017
Biotransformation Tamponnet et al., 2008
Complexation
Bio-crystallisation Reena et al., 2012
Dissolution and speciation Francis and Dodge, 2009

soil thus, severely affecting adsorption of radiocaesium. Bio- characteristics of the bacteria present (Tisa

kova

et al., 2013). Size
accumulation process can be either active or passive. Active bio- and lipid content also influences it, with a decrease in size leading
accumulation is a relatively slower process, requires more energy to less surface area for accumulation. (Jorgensen, 2010). Presence of
and can be dependent or independent of metabolism. Passive capsule or slime or S-layers dramatically influences the bio-
bioaccumulation had been found to be more favorable in areas with accumulation process. Once accumulated, the nuclides are being
nutrient limitation. It is also faster and less energy consuming than acted up on by polyphosphate bodies. Such intracellular chelation
active process. (Haferburg and Kothe, 2007). Accumulation could mechanisms have suggested to give rise to metal and subsequent
be either intracellular or extracellular. Intracellular accumulation of radionuclide tolerance (Keasling and Hupf, 1996). However, Jiang
radionuclides could be attributed directly to the presence or et al. (2004) stated that, it is the surface characteristics of the
absence of the respective radionuclide transporter, effect of nuclide bacterial cell wall-which determines its adsorption properties. The
on permeability of the cell membrane. (Merroun and Selenska- differences in cell wall composition in Gram-positive and Gram-
Pobell, 2008). A study by Francis et al. (2004) showed that intra- negative bacteria showed little to no significance on bio-
cellular accumulation of U(VI) in Citrobacter sp. and Halomonas sp. accumulation capability.
was largely in form of phosphates such as; hydroxophosphate or
polyphosphates or as uranium hydrogen phosphate. Accumulation 3.3.2. Biosorption
of iodide on soil Bacillus subtilis cell wall were found to intensify up Prakash et al. (2013) described the phenomenon of biosorption
on addition of glucose. (Amachi et al., 2005). Bacillus vallismortis as, “the sequestration of positively charged metal ions to the negatively
showed to bioaccumulate U(VI) at 5 mg/L concentration after 72 h charged cell membranes and polysaccharides secreted on the outer
of inoculation. About 50 mg/g (metal/dry bacteria) U(VI) was surfaces of bacteria”. Bacterial cell wall comprise peptidoglycan or
accumulated which was later determined by UVeVis spectropho- lipopolysaccharide, for Gram positive and Gram-negative bacteria
tometry (Ozdemir et al., 2017). An interesting research on radio- respectively. However, owing to the phosphate moiety there exists
nuclide exchange between uranium and a proton was determined an electronegative membrane charge to which positive cations of
using a separation factor and it was revealed that, members of metals and radionuclides are attracted. Such attraction force leads
Gram-positive bacteria namely, Micrococcus luteus, B. subtilis and to adsorption of the nuclides on to the surface of the cell. Bio-
B. megatarium showed potential for accumulation of Th in a solu- sorption can occur directly, by interaction of nuclide cation with
tion containing Th and U. (Tsuruta, 2006). anionic cell wall functional groups or it could be indirect, with
Since bioaccumulation involves rapid interactions with anionic either EPS, S-layer or capsule. Since the binding of nuclides with cell
groups present in components of cell surface, it is significantly wall could also be due to ligands such as, carboxyl, amine, hydroxyl,
affected by molecular properties of the nuclide, properties and phosphate etc., it is described as a passive uptake process (Merroun
 A. Shukla et al. / Journal of Environmental Radioactivity 180 (2017) 27e35 31

and Selenska-Pobell, 2008 and Luk'yanova et al., 2008). Bacterial reduction of radionuclides, the reduction of radionuclide is con-
strains capable of accumulating 60Co, 89Sr, 106Ru, 131I, 135Cs and current to energy metabolism. It includes use of a substance as an
144
Ce had been acknowledged with the help of autoradiography electron acceptor for generation of energy. The electron acceptor is
technique (Kokke et al., 1969). Extracellular polymeric substance reduced but not incorporated into an organic matter during the
(EPS) obtained from Rhodococcus opacus and R. rhodochrous had biosynthetic anabolism process (Lloyd and Lovley, 2001). The
been used as sorbents for the sorption of Cd(II), Pb(II), Ni(II), Co(II) biggest bottleneck of this process is that it is, exclusive to obligate
and Cr(VI) ions. Biosorption leads to immobilization of the radio- anaerobes. (Gadd, 1996). Addition of riboflavin has proven to
nuclide. The process is species specific and, is influenced by tem- enhance microbial reduction rates of Tc(VI), Np(V) and Pu(IV) by
perature, aeration, pH, phase of growth of cells, secretion or Shewanella oneidensis (Cherkouk et al., 2016). The same study
production of exopolymers; presence of organic or inorganic con- concluded that riboflavins could be very well be used to signifi-
tent and metabolites. Electrostatic attraction, chemical interaction cantly accelerate the process of bioremediation of radionuclide
of extracellular biopolymers and functional groups as well as metal containing waste.
ions also influence biosorption (Dobrowolski et al., 2017). Xie et al.
(2008) observed in their study, that carboxyl present in cell wall of 3.3.4. Biosolubilisation
Citrobacter freudii served as one of the active sites for biosorption Biosolubilisation is a result of autotrophic metabolism during
and exhibited significant effect on sorption. They concluded that which, radionuclides are leached out from their solid matrices
since dead cells exhibit better sorption ability, the entire process (Gadd, 2002). It is an indirect method of solubilisation as the
was influence by the presence of functional groups in cell wall than autotrophic bacteria obtain energy from reduced Fe or S com-
any other biological activity of the cell. The biggest shortcomings of pounds whilst solubilizing the nuclides and metals. It requires
biosorption are; quick saturation with nuclide molecules and acidic pH, moisture and oxygen to oxidise Fe, S and leach out metals
competitive desorption occurring due to cations, other than the as sulfides. Such bacteria are mesophilic and acidophilic in nature
desired one, for binding site on to the cell (Jabbar and Wallner, (Ghauri and Johnson, 1991). Usually, a mixture of acid and bacteria
2015). Hence, biosorption is generally applied for removal of low along with an inorganic source of energy is added to mines of
concentration radionuclides from effluents (Merroun and Selenska- metals and radionuclides, after the application of physical, chemical
Pobell, 2008). and other hydrometallurgical process for solubilisation (Pandey
and Natarajan, 2015). Acidithiobacillus ferrooxidans, Aciditiobacillus
3.3.3. Biotransformation thiooxidans, Leptospirillum ferrooxidans, Sulfolobus (Ewart and
Bioavailability and concentration of radionuclides can be Hughes, 1991; Bosecker, 1997; Munoz et al., 1995) have been re-
dramatically altered by bacterial processes (Francis, 2007). Redox ported to solubilse metals.
reactions lead to a change in solubility of the nuclides, pH revises It is affected by the oxidation state of the nuclide, pH sur-
their solubility (Francis and Nancharaiah, 2015). Thus, key chemical rounding the bacteria, moisture and inorganic content as substrate
processes by bacterial transformations lead to formation of oxides, for the bacteria. Presence of citrate, a crucial bacterial metabolite,
coprecipitates, ionic, organic or inorganic complexes of radionu- leads to an increase in solubility of nuclides for an extended period
clides (Francis and Dodge. 2009). Both, the aerobic and anaerobic of time. However, uranyl citrate complex dissociates in conditions
bacteria that are actively growing, possess the ability of biotrans- with greater salinity and presence of phosphate-leading to pre-
formation via redox reactions. Usually, non-sorptive nuclides are cipitation of uranium and citric acid. Thus, citric acid acts as a
either transformed enzymatically or non-enzymatically. Microbes crucial effector in the process of biosolubilisation (Francis et al.,
possess the ability to utilize oxidised form of radionuclides and 1992).
metals such as U, Tc, Cr as terminal electron acceptor (TEA). Oxi-
dised form of such nuclides are water-soluble and mobile while 3.3.5. Bioprecipitation
their reduction results in their precipitatation. Soluble forms of U, Precipitation results after successful conversion of soluble form
Tc and Cr are U(VI), Tc(VIII) and Cr(VI) respectively (Tabak et al., of a nuclide into its insoluble form. In case of radionuclides, as
2005; Lovley, 2002). The reported bacteria and archaea that mentioned above, their reduced forms are highly insoluble-
dominate biotransformation reactions are those capable of resulting in their precipitation. Precipitation of metals and radio-
dissimilatory Fe(II) or sulphate-reducing bacteria (DIRB and DSRB), nuclides occur mostly as carbonates or hydroxides. The importance
for example, Geobacter sulfurreducens strain PCA and Anaeromyx- of oxidation state and valence of the radionuclide in bio-
obacter dehalogenans strain K and Shewanella putrefaciencs strain precipitation remains undisputed. The site of precipitation on mi-
CN-32. Bioreduction and bioprecipitation ultimately results in crobial cell is known as the ‘nucleation site’ and it depends on the
immobilization of the radionuclide (O'Loughlin et al., 2011; Rui concentration of ligand produced by the cell. Microbially produced
et al., 2013). Role of triheme periplasmic cytochrome type-c had ligands and biogenic formation of minerals influence precipitation
been identified to be a crucial for biotransformation (Jabbar and of the radionuclide (Jabbar and Wallner, 2015). Bacterial secretions
Wallner, 2015). Differences in direct and indirect bacterial reduc- and metabolism can lead to a localized change in pH, Eh in its
tion of radionuclides is depicted in Figs. 2 and 3. surrounding thus, also changing the pH of the immediate vicinity of
Enzymatic reduction of metals and radionuclides has been the metal. (Merroun and Selenska-Pobell, 2008). Co-precipitation is
extensively observed in bacteria such as; Shewanella oneidensis, S. another interesting phenomenon where elements are amalgam-
putrefacriens, Geobacter metallireducens. Reduction of Tc has been ated in metal oxide minerals during their precipitation (Tabak et al.,
reported under varying pH conditions, parallel to formation of H2O 2005).
during metabolism (Jabbar and Wallner, 2015). Anaerobic reductive
dissolution of Pu(IV)-Pu(III) by Bacillus sp., S. marcescens, Clos- 3.3.6. Miscellaneous
tridium sp. has been reported by (Francis, 2007). A highly non- 3.3.6.1. Chelation. Microbial production of chelating biopolymers,
sorptive radionuclide Np(V) undergoes anaerobic bioreduction such as pyomelanin, melanin etc. have shown to modify the
and biomineralization processes in presence of either hydrogen, mobilization of radionuclides significantly (Tamponnet et al.,
pyruvate or citrate (Rittmann et al., 2002; Mohapatra et al., 2010). 2008). Exposure of such melanin to ionizing radiation has also
Desulfovibrio desulfuricans has been reported by Icopini et al. (2007) demonstrated an increase in growth and biomass in fungi; Cryp-
to successfully carry out reduction of Np(V). In dissimilatory tococcus neoformans, Wangiella dematitidis and Cladosporium
32 A. Shukla et al. / Journal of Environmental Radioactivity 180 (2017) 27e35

Fig. 2. Direct enzymatic reduction of radionuclides by bacteria.

Bacteria use electrons released during reduction of organic compounds (substrate) to convert oxidised, mobile and soluble forms of radionuclides such as U, Cr or Tc into reduced,
immobile and their respective insoluble forms. Species of Desulfovibrio and Shewanella have demonstrated precipitation of U in presence of c-type cytochrome using acetic acid,
ethanol, lactic acid, hydrogen etc. act as substrate.
(Source: Tabak et al., 2005; Jabbar and Wallner, 2015).

Fig. 3. Indirect reduction of radionuclides

Some bacteria, mostly lithotrophs, cause reduction of substance, which in turn lead to reduction of radionuclides. Since there is no direct enzymatic reduction of radionuclide by
bacteria, it has been called an indirect reduction mechanism. Role of cyctochrome c7, PpcA in iron-reducing bacteria (IRB) has been studied.
(Source: Jabbar and Wallner, 2015).

sphaerospermum (Dadachova et al., 2007). Synthesis of metabolic ecotoxicological concern. Microbes possess an immense potential
byproducts, such as siderophores, have been widely studied on for undergoing sustainable manipulations for biotechnological
pseudomonads (Meyer, 2000). reported production of a fluorescent applications. It is hence palpable to use microbes in removal of
siderophore pyoverdin by P. grimontii. However, siderophore pro- radionuclides from environment. Some typical processes involved
duction exhibiting considerable sorption capacity, by P. fluorescens have been summarized in Table 3. Natural attenuation involves on
and P. stutzerii in presence of radionuclides 147Pm, 234Th and 241Am the intrinsic bioremediation potential without any human inter-
was studied by Arlinger et al. (2003). Such studies shed light on vention and-being recalcitrant and persisting in nature, radionu-
mobilization of radionuclides in groundwater. clides have been the cause of concern for the scientific community
(Francis and Nancharaiah, 2015). Ultimately, it were the indigenous
3.3.6.2. Complexation. Complexation results when organic phos- bacteria that rose to the occasion and have since been subjected to
phate groups and teichoic acid and radionuclides interact with each extreme scrutiny for their potential biotechnological application.
other. U(VI), for example, can be complexed on to the cell wall of Radionuclides cannot be destroyed but can only be transformed.
Gram-positive bacteria since they are relatively rich in teichoic acid The ones with greater solubility can be immolibilized while those
content, in contrast to Gram-negative bacteria. Gadd (2002) states with lesser solubility can be flushed out. A change in immediate
the complexation of Co2þ by citric acid, a bacterial metabolite. vicinity of the radionuclide can aide in modifying the solubility of
Nutrient transporter-analogue of K was reported to transport Cs137 radionuclides (Hazen and Tabak, 2005). Turick and Berry (2016)
into the cell (Shaw, 2005; Bennett and Willey, 2003). Speciation reviewed microbial activity involved in degradation of concrete
and binding of radionuclides to fungal cells influences its precipi- where, nuclear waste was bring stored. A comprehensive compi-
tation capabilities. Thus, retention of Cs in forest soil had been lation of database of bacteria and fungi, wild type or recombinant,
accredited to mobilization, uptake and translocation of radionu- which are been used in remediation of radioactive waste, has been
clides and nutrient by fungi (Steiner et al., 2002). Sequestration of created as ‘BioRadBase’ (Reena et al., 2012). Xu and Zhou (2017)
Sr in Serattia sp. produced hydroxyapatite was reported by enlists the significant advantages in using microbes for remedia-
(Handley-Sidhu et al., 2011a,b). Complexing agents include tion of radioactive waste are:
ethylene diamine tetra acetate (EDTA), diethylene triamine penta
acetic acid (DTPA), oxalate, citrate, humic acid, fulvic acids, bi- (a) High specificity
carbonates etc. (Luo and Gu, 2011; Wan et al., 2008). (b) High reusability
(c) High efficiency
(d) Complete removal of pollutant
4. Microbial remediation of radionuclides
(e) Low expense
(f) No secondary pollution
Exposure to radionuclides is a health as well as an
 A. Shukla et al. / Journal of Environmental Radioactivity 180 (2017) 27e35 33

Table 3
Mechanisms of radionuclide microbial bioremediation.

Mechanism/Process Radionuclide/Metal Microbe involved Reference

Metabolism-dependent  Sulphide precipitation U(VI), Ga(III), Cr(III), Pu(IV), Sc, Shewanella putrefaciens Gadd, 1996
 Transport In, Ni, U, Th Desulfovibrio desulfuricans
 Intracellular compartmentation Desulfotomaculum sp.
 Sequestration by proteins, peptides Geobacter metallireducens
 Immobilization by chemical reduction Aspegillus niger
 Siderophore complexation
Enzymatic  Direct U(VI) G. sulfurreducens, Clostridium Merroun and Selenska-Pobell,
 Indirect sp., S. putrefaciencs, 2008; Francis and Dodge, 2009;
Desulfovibrio vulgaris, D. Lovley, 2002; Prakash et al.,
desulfuricans 2013; Prakash et al., 2013;
Biomineralization Cr As sulphides, phosphates Citrobacter, Acinetobacter Lloyd and Lovley, 2001; Hazen
johnsonii, Klebsiella planticola, and Tabak, 2005.
Pseudomonas aeruginosa, P.
putida, Salmonella enterica,
Escherichia coli
Biostimulation Pu(IV), U(VI), Np(V), Tc(VII) Geobacter, Arthrobacter ilicis
Bioaugmentation
Dissimilatory reduction Hg(II), As(V), Fe(III), U(VI), Streptomyces, Aciditiobacillus
Tc(VII), Cr(VI), Co(III), Cr(VI), ferrooxidans, P. putida, Ralstonia
Tc(VII), eutropha, Pyrobaculum
islandicum, Geobacter,
Sulfospirillum barnesii,
Rhodanobacter sp.,
Desulfuromusa ferrireducens,
Deinococcus radiodurans,
Sulfurospirillum barnesii
Detoxification Hg(II) Streptomyces sp., Thiobacillus
ferrooxidans, P. putida, Ralstonia
eutropha,
Biotransformation Pb(II), Zn(II), Cd(II), Sr(II), Th, Pseudomonas mendocina, Hazen and Tabak., 2005;
Biosorption U(IV) Bacillus subtilis, Arthrobacter Haferburg and Kothe, 2007; Yin
Bioaccumulation spp., Rhizopus arrhizus, A. et al., 2017; Suzuki and
nicotianae, Micrococcus luteus, Banfield, 2004; Sheppard et al.,
B. vallismortis 2009; Ozdemir et al., 2017
Biodegradation of chelators
Volatilization
Treatment trains
Natural attenuation A. ilicis Suzuki and Banfield, 2004
Bioprecipitation Uranyl phosphate D. radiodurans Suzuki and Banfield, 2004
Genetically modified microorganisms Uranyl nitrate, cobalt, Hg(II) D. radiodurans R1, Escherichia Amachi et al., 2005;
coli, R. eutropha, Alexandrova et al., 2011;
Groudev et al., 2001; Prakash et
al., 2013; Lloyd and Lovley,
2001.

Addition of specific strains that are able to carry out desired that, the beads could be easily recovered and reused without any
microbial activity, to a sample is called bioaugmentation (Xu and prominent loss of efficiency (Sasaki et al., 2015). Mumtaz et al.
Zhou, 2017). The application of microorganisms in bioremediation (2013) carried out an interesting study which concluded the
of radionuclides is limited to their ability to tolerate, survive and growth of fungi subjugates bacteria in presence of high concen-
resist high levels of radiation while simultaneously carrying out the trations of radionuclides.
desired function (Brim et al., 2000). In situ approach of bioreme- Regardless of the processes or mechanisms involved, bacteria
diation in marine sediments have been discussed by Lofrano et al. have established themselves as an alternative to the conventional
(2016). In bioremediation; bioaugmentation, biostimulation, bio- techniques of radiation and heavy metal nuclide remediation. It is a
mineralization and dissimilatory reduction have been extensively matter of time when their true potential is recognized and the first
used (Hazen and Tabak, 2005; Lloyd and Lovley, 2001). It has been step in achieving their potential is knowing their varying ways of
noted that immobilization and precipitation play a significant role interaction with them.
in remediation of metal and radionuclide contaminated sites (Islam
and Sar, 2011). Development of a ‘bio-inorganic ion exchanger’ has 5. Challenges and future prospects
shown promising results in removal of about 97% of Cs137 and 85%
of Co60 over the course of 7 days, as reported by Paterson-Beedle There exists no reservations that microbes, specifically bacteria
et al. (2006). The experiment made us of immobilized biofilm of and archaea, possess tremendous knack to not only withstand
Serratia sp. coated with hydrogen uranyl phosphate. Removal of extreme conditions but also carry out important biotechnological
radionuclides was facilitated by intercalation of target species onto processes. Contrary to their microscopic size, they have relentlessly
a polyurethane foam matrix. Hence, the mechanism of removal shown to carry out certain vital and unique processes without
relied on the fundamental principles of cation exchange intercala- which other life might not be able to sustain or even exist. The
tion. Immobilized arginate beads containing photosynthetic bac- microbes have shown their ability to undergo genetic manipula-
teria Rhodobacter sphaeroides showed to remove 59e74% Cs from tions and carry out their recombinant phenotypic traits. It is also
soil as well as sediment mud. The advantage of the method was interesting to note that the interaction mechanisms with
34 A. Shukla et al. / Journal of Environmental Radioactivity 180 (2017) 27e35

radionuclides, as discussed extensively in this review, are akin to radionuclides. In: Paper Presented at the Submitted to the 9th Biennial DAE-
BRNS Symposium on Nuclear and Radio-chemistry (NUCAR02009).
those of metals. Recently, the biotechnological applications of re-
Francis, A., Dodge, C., Gillow, J., 1992. Biodegradation of Metal Citrate Complexes
combinant bacteria have shown encouraging results in remediation and Implications for Toxic-metal Mobility.
of radwaste. It seems only prudent to make use of those microbes Gadd, G., 1996. Influence of microorganisms on the environmental fate of radio-
that are indigenous to radionuclide containing natural samples, nuclides. Endeavour 20 (4), 150e156.
Gadd, G.M., 2002. Microbial interactions with metals/radionuclides: the basis of
such as soil, air or water, and subject them to extreme scrutiny for bioremediation. Radioact. Environ. 2, 179e203.
exploring their capabilities. True potential of these microbial pro- Gazso
, L.G., 2001. The key microbial processes in the removal of toxic metals and
cesses can be unlocked by frequent and sustaining collaborations radionuclides from the environment. Central Eur. J. Occup. Environ. Med. 7 (3/
4), 178e185.
with various fields of science and technology and, once character-
mez-Zavaglia, A., 2015. Role of S-
Gerbino, E., Carasi, P., Mobili, P., Serradell, M.A., Go
ized completely; these microscopic beings can be used, in isolation layer proteins in bacteria. World J. Microbiol. Biotechnol. 31 (12), 1877e1887.
or as a consortia, for removal of high concentrations of radwaste. Ghauri, M.A., Johnson, D.B., 1991. Physiological diversity amongst some moderately
thermophilic iron-oxidising bacteria. FEMS Microbiol. Lett. 85 (4), 327e333.
The removed radionuclide can be further used as substrate for Groudev, S., Georgiev, P., Spasova, I., Komnitsas, K., 2001. Bioremediation of a soil
other commercial applications. The beauty of using microbes for contaminated with radioactive elements. Hydrometallurgy 59 (2), 311e318.
the job lies in their reusability. Such an approach could lead to the Haferburg, G., Kothe, E., 2007. Microbes and metals: interactions in the environ-
ment. J. basic Microbiol. 47 (6), 453e467.
development of an eco-friendly way for treatment as well as Handley-Sidhu, S., Renshaw, J.C., Yong, P., Kerley, R., Macaskie, L.E., 2011a. Nano-
extraction and/or recovery of precious radionuclides. crystalline hydroxyapatite bio-mineral for the treatment of strontium from
aqueous solutions. Biotechnol. Lett. 33 (1), 79e87.
Handley-Sidhu, S., Renshaw, J., Moriyama, S., Stolpe, B., Mennan, C., Bagheriasl, S.,
References et al., 2011b. Uptake of Sr2þ and Co2þ into biogenic hydroxyapatite: implica-
tions for biomineral ion exchange synthesis. Environ. Sci. Technol. 45 (16),
Alexandrova, M., Rozhko, T., Vydryakova, G., Kudryasheva, N., 2011. Effect of 6985e6990.
americium-241 on luminous bacteria. Role of peroxides. J. Environ. Radioact. Hazen, T.C., Tabak, H.H., 2005. Developments in bioremediation of soils and sedi-
102 (4), 407e411. ments polluted with metals and radionuclides: 2. Field research on bioreme-
Amachi, S., Fujii, T., Shinoyama, H., Muramatsu, Y., 2005. Microbial influences on the diation of metals and radionuclides. Rev. Environ. Sci. Biotechnol. 4 (3),
mobility and transformation of radioactive iodine in the environment. J. Nucl. 157e183.
Radiochem. Sci. 6 (1), 21e24. Hitoshi, I., Watanabe, H., Takehisa, M., Iizuka, H., 1983. Isolation and identification of
Arlinger, J., Oskarsson, A., Albinsson, Y., Andlid, T., Pedersen, K., 2003. Mobilisation radiation-resistant cocci belonging to the genus Deinococcus from sewage
of radionuclides by ligands produced by bacteria from the deep subsurface. In: sludges and animal feeds. Agric. Biol. Chem. 47 (6), 1239e1247.
Paper Presented at the MRS Proceedings. IAEA, 2017. Radiation Technology the Industrial Revolution behind the Scenes. IAEA
Bennett, R., Willey, N., 2003. Soil availability, plant uptake and soil to plant transfer Bulletin (March) 58e1. International Atomic Energy Agency, Vienna.
of 99 Tcda review. J. Environ. Radioact. 65 (2), 215e231. Icopini, G.A., Boukhalfa, H., Neu, M.P., 2007. Biological reduction of Np (V) and Np
Bosecker, K., 1997. Bioleaching: metal solubilization by microorganisms. FEMS (V) citrate by metal-reducing bacteria. Environ. Sci. Technol. 41 (8), 2764e2769.
Microbiol. Rev. 20 (3e4), 591e604. Islam, E., Sar, P., 2011. Culture-dependent and-independent molecular analysis of
Brim, H., McFarlan, S.C., Fredrickson, J.K., Minton, K.W., Zhai, M., Wackett, L.P., the bacterial community within uranium ore. J. basic Microbiol. 51 (4),
Daly, M.J., 2000. Engineering Deinococcus radiodurans for metal remediation in 372e384.
radioactive mixed waste environments. Nat. Biotechnol. 18 (1), 85e90. Jabbar, T., Wallner, G., 2015. Biotransformation of Radionuclides: Trends and Chal-
Cherkouk, A., Law, G.T., Rizoulis, A., Law, K., Renshaw, J.C., Morris, K., et al., 2016. lenges Radionuclides in the Environment. Springer, pp. 169e184.
Influence of riboflavin on the reduction of radionuclides by Shewanella onei- Jiang, W., Saxena, A., Song, B., Ward, B.B., Beveridge, T.J., Myneni, S.C., 2004. Eluci-
denis MR-1. Dalton Trans. 45 (12), 5030e5037. dation of functional groups on gram-positive and gram-negative bacterial
Choudhary, S., Sar, P., 2011. Identification and characterization of uranium accu- surfaces using infrared spectroscopy. Langmuir 20 (26), 11433e11442.
mulation potential of a uranium mine isolated Pseudomonas strain. World J. Jorgensen, E., 2010. Ecotoxicology. Elsevier Science.
Microbiol. Biotechnol. 27 (8), 1795e1801. Keasling, J., Hupf, G.A., 1996. Genetic manipulation of polyphosphate metabolism
Choudhary, S., Islam, E., Kazy, S.K., Sar, P., 2012. Uranium and other heavy metal affects cadmium tolerance in Escherichia coli. Appl. Environ. Microbiol. 62 (2),
resistance and accumulation in bacteria isolated from uranium mine wastes. 743e746.
Part A J. Environ. Sci. Health 47 (4), 622e637. Kokke, R., Zuilekom, J.T., Wike
n, T., 1969. Detection and isolation of radionuclide-
Cox, M.M., Battista, J.R., 2005. Deinococcus radioduransdthe consummate survivor. accumulating bacteria by autoradiography. Antonie Leeuwenhoek 35 (1),
Nat. Rev. Microbiol. 3 (11), 882e892. 121e128.
Dadachova, E., Casadevall, A., 2008. Ionizing radiation: how fungi cope, adapt, and Krabbenhoft, K., Anderson, A., Elliker, P., 1965. Ecology of Micrococcus radiodurans.
exploit with the help of melanin. Curr. Opin. Microbiol. 11 (6), 525e531. Appl. Microbiol. 13 (6), 1030e1037.
Dadachova, E., Bryan, R.A., Huang, X., Moadel, T., Schweitzer, A.D., Aisen, P., et al., Krupka, K.M., Kaplan, D., Whelan, G., Serne, R., Mattigod, S., 1999. Understanding
2007. Ionizing radiation changes the electronic properties of melanin and en- Variation in Partition Coefficient, Kd, Values. Volume II: Review of Geochem-
hances the growth of melanized fungi. PloS One 2 (5), e457. istry and Available Kd Values, for Cadmium, Cesium, Chromium, Lead, Pluto-
Daly, M.J., Gaidamakova, E.K., Matrosova, V., Vasilenko, A., Zhai, M., nium, Radon, Strontium, Thorium, Tritium (3H), and Uranium. EPA.
Venkateswaran, A., et al., 2004. Accumulation of Mn (II) in Deinococcus radi- Lloyd, J.R., Lovley, D.R., 2001. Microbial detoxification of metals and radionuclides.
odurans facilitates gamma-radiation resistance. Science 306 (5698), Curr. Opin. Biotechnol. 12 (3), 248e253.
1025e1028. Lloyd, J.R., Renshaw, J.C., 2005. Bioremediation of radioactive waste: radio-
Dekker, L., Osborne, T.H., Santini, J.M., 2014. Isolation and identification of cobalt- nuclideemicrobe interactions in laboratory and field-scale studies. Curr. Opin.
and caesium-resistant bacteria from a nuclear fuel storage pond. FEMS Micro- Biotechnol. 16 (3), 254e260.
biol. Lett. 359 (1), 81e84. Lofrano, G., Libralato, G., Minetto, D., De Gisi, S., Todaro, F., Conte, B., et al., 2016. In
Dhal, P.K., Sar, P., 2014. Microbial communities in uranium mine tailings and mine situ remediation of contaminated marinesediment: an overview. Environ. Sci.
water sediment from Jaduguda U mine, India: a culture independent analysis. Pollut. Res. 1e18.
Part A J. Environ. Sci. Health 49 (6), 694e709. Lovley, D.R., 2002. Microbial redox interactions with uranium: an environmental
Dhawal, S., Phadatare, M., Thorat, N., Kulkarni, G., Pawar, S., 2013. Natural radio- perspective. Radioact. Environ. 2, 205e223.
activity study in soil samples of South Konkan, Maharashtra, India. Radiat. Prot. Luk’yanova, E., Zakharova, E., Konstantinova, L., Nazina, T., 2008. Sorption of ra-
Dosim. 157 (2), 225e233. dionuclides by microorganisms from a deep repository of liquid low-level
Dobrowolski, R., Szcze
s, A., Czemierska, M., Jarosz-Wikołazka, A., 2017. Studies of waste. Radiochemistry 50 (1), 85e90.
cadmium (II), lead (II), nickel (II), cobalt (II) and chromium (VI) sorption on Luo, W., Gu, B., 2011. Dissolution of uranium-bearing minerals and mobilization of
extracellular polymeric substances produced by Rhodococcus opacus and uranium by organic ligands in a biologically reduced sediment. Environ. Sci.
Rhodococcus rhodochrous. Bioresour. Technol. 225, 113e120. Technol. 45 (7), 2994e2999.
Ewart, D.K., Hughes, M.N., 1991. The extraction of metals from ores using bacteria. Merroun, M.L., Selenska-Pobell, S., 2008. Bacterial interactions with uranium: an
Adv. Inorg. Chem. 36, 103e135. environmental perspective. J. Contam. Hydrology 102 (3), 285e295.
Francis, A., 2007. Microbial mobilization and immobilization of plutonium. J. Alloys Meyer, J.-M., 2000. Pyoverdines: pigments, siderophores and potential taxonomic
Compd. 444, 500e505. markers of fluorescent Pseudomonas species. Archives Microbiol. 174 (3),
Francis, A.J., Nancharaiah, Y.V., 2015. In situ and ex situ bioremediation of 135e142.
radionuclide-contaminated soils at nuclear and norm sites. Environ. Remediat. Michalik, B., 2017. NORM contaminated area identification using radionuclides ac-
Restor. Contam. Nucl. NORM Sites 185e236. tivity concentration pattern in a soil profile. J. Environ. Radioact. 169, 9e18.
Francis, A.J., Gillow, J., Dodge, C.J., Harris, R., Beveridge, T., Papenguth, H., 2004. Misra, H.S., Khairnar, N.P., Kota, S., Shrivastava, S., Joshi, V.P., Apte, S.K., 2006. An
Uranium association with halophilic and non-halophilic bacteria and archaea. exonuclease I-sensitive DNA repair pathway in Deinococcus radiodurans: a
Radiochim. Acta 92 (8), 481e488. major determinant of radiation resistance. Mol. Microbiol. 59 (4), 1308e1316.
Francis, A., Dodge, C., 2009. Microbial transformation of actinides and other Mohapatra, B.R., Dinardo, O., Gould, W.D., Koren, D.W., 2010. Biochemical and
 A. Shukla et al. / Journal of Environmental Radioactivity 180 (2017) 27e35 35

genomic facets on the dissimilatory reduction of radionuclides by micro- radioactive contaminated soil remediation technologies and selection princi-
organismseA review. Miner. Eng. 23 (8), 591e599. ples. In: Jiang, H. (Ed.), Proceedings of the 20th Pacific Basin Nuclear Confer-
Mumtaz, S., Streten-Joyce, C., Parry, D.L., McGuinness, K.A., Lu, P., Gibb, K.S., 2013. ence, vol. 3. Springer Singapore, Singapore, pp. 547e554.
Fungi outcompete bacteria under increased uranium concentration in culture Shaw, G., 2005. Applying radioecology in a world of multiple contaminants.
media. J. Environ. Radioact. 120, 39e44. J. Environ. Radioact. 81 (2), 117e130.
Munoz, J., Gonzalez, F., Blazquez, M., Ballester, A., 1995. A study of the bioleaching of Sheppard, S., Long, J., Sanipelli, B., Sohlenius, G., 2009. Solid/liquid Partition Co-
a Spanish uranium ore. Part I: a review of the bacterial leaching in the treat- efficients (Kd) for Selected Soils and Sediments at Forsmark and Laxemar-
ment of uranium ores. Hydrometallurgy 38 (1), 39e57. simpevarp: Svensk K€ arnbr€
anslehantering (SKB).
Narayana, Y., Somashekarappa, H., Karunakara, N., Avadhani, D., Mahesh, H., Staunton, S., Dumat, Camille, Zsolnay, A., 2002. Possible role of organic matter in
Siddappa, K., 2001. Natural radioactivity in the soil samples of Coastal Karna- radiocaesium adsorption in soils. J. Environ. Radioact. 58.2, 163e173.
taka of South India. Health Phys. 80 (1), 24e33. Steiner, M., Linkov, I., Yoshida, S., 2002. The role of fungi in the transfer and cycling
O'Loughlin, E.J., Boyanov, M.I., Antonopoulos, D.A., Kemner, K.M., 2011. Redox Pro- of radionuclides in forest ecosystems. J. Environ. Radioact. 58 (2), 217e241.
cesses Affecting the Speciation of Technetium, Uranium, Neptunium, and Suzuki, Y., Banfield, J.F., 2004. Resistance to, and accumulation of, uranium by
Plutonium in Aquatic and Terrestrial Environments Aquatic Redox Chemistry. bacteria from a uranium-contaminated site. Geomicrobiol. J. 21 (2), 113e121.
ACS Publications, pp. 477e517. Tabak, H.H., Lens, P., van Hullebusch, E.D., Dejonghe, W., 2005. Developments in
Ozdemir, S., Oduncu, M.K., Kilinc, E., Soylak, M., 2017. Resistance, bioaccumulation bioremediation of soils and sediments polluted with metals and radio-
and solid phase extraction of uranium (VI) by Bacillus vallismortis and its nuclidese1. Microbial processes and mechanisms affecting bioremediation of
UVevis spectrophotometric determination. J. Environ. Radioact. 171, 217e225. metal contamination and influencing metal toxicity and transport. Rev. Environ.
Pandey, B., Natarajan, K., 2015. Microbiology for Minerals, Metals, Materials and the Sci. Biotechnol. 4 (3), 115e156.
Environment. CRC Press. Tamponnet, C., Martin-Garin, A., Gonze, M.-A., Parekh, N., Vallejo, R., Sauras-Yera, T.,
Paterson-Beedle, M., Macaskie, L.E., Lee, C.H., Hriljac, J.A., Jee, K.Y., Kim, W.H., 2006. et al., 2008. An overview of BORIS: bioavailability of radionuclides in soils.
Utilisation of a hydrogen uranyl phosphate-based ion exchanger supported on a J. Environ. Radioact. 99 (5), 820e830.
biofilm for the removal of cobalt, strontium and caesium from aqueous solu- Tisa

kov
a, L.E.N.K.A., Pipíska, M.A.R.T.I.N., Goda
ny, A.N.D.R.E.J.,
tions. Hydrometallurgy 83 (1), 141e145. Horník, M.I.R.O.S.L.A.V., Vidova
, B., Augustín, J., 2013. Bioaccumulation of 137Cs
Prakash, D., Gabani, P., Chandel, A.K., Ronen, Z., Singh, O.V., 2013. Bioremediation: a and 60Co by bacteria isolated from spent nuclear fuel pools. J. Radioanalytical
genuine technology to remediate radionuclides from the environment. Microb. Nucl. Chem. 295 (1), 737e748.
Biotechnol. 6 (4), 349e360. Tsuruta, T., 2006. Bioaccumulation of uranium and thorium from the solution
Prescott, L., Hardy, M., Klein, J., 2006. Microbiology 8TH Edition McGraw Hill New containing both elements using various microorganisms. J. Alloys Compd. 408,
York. 1312e1315.
Ravanat, J.-L., Douki, T., 2016. UV and ionizing radiations induced DNA damage, Turick, C.E., Berry, C.J., 2016. Review of concrete biodeterioration in relation to
differences and similarities. Radiat. Phys. Chem. 128, 92e102. nuclear waste. J. Environ. Radioact. 151, 12e21.
Ravisankar, R., Vanasundari, K., Chandrasekaran, A., Rajalakshmi, A., Suganya, M., Van Hullebusch, E.D., Lens, P.N., Tabak, H.H., 2005. Developments in bioremediation
Vijayagopal, P., Meenakshisundaram, V., 2012. Measurement of natural radio- of soils and sediments polluted with metals and radionuclides. 3. Influence of
activity in building materials of Namakkal, Tamil Nadu, India using gamma-ray chemical speciation and bioavailability on contaminants immobilization/
spectrometry. Appl. Radiat. Isotopes 70 (4), 699e704. mobilization bio-processes. Rev. Environ. Sci. Bio/Technology 4 (3), 185e212.
Reena, R., Majhi, M.C., Arya, A.K., Kumar, R., Kumar, A., 2012. BioRadBase: a database Venkateswaran, A., McFarlan, S.C., Ghosal, D., Minton, K.W., Vasilenko, A.,
for bioremediation of radioactive waste. Afr. J. Biotechnol. 11 (35), 8718e8721. Makarova, K., et al., 2000. Physiologic determinants of radiation resistance
Rittmann, B.E., Banaszak, J.E., Reed, D.T., 2002. Reduction of Np (V) and precipitation inDeinococcus radiodurans. Appl. Environ. Microbiol. 66 (6), 2620e2626.
of Np (IV) by an anaerobic microbial consortium. Biodegradation 13 (5), Wan, J., Tokunaga, T.K., Kim, Y., Brodie, E., Daly, R., Hazen, T.C., Firestone, M.K., 2008.
329e342. Effects of organic carbon supply rates on uranium mobility in a previously
Rodrigue, A., Effantin, G., Mandrand-Berthelot, M.A., 2005. Identification of rcnA bioreduced contaminated sediment. Environ. Sci. Technol. 42 (20), 7573e7579.
(yohM), a nickel and cobalt resistance gene in Escherichia coli. J. Bacteriol. 187 Xie, S., Yang, J., Chen, C., Zhang, X., Wang, Q., Zhang, C., 2008. Study on biosorption
(8), 2912e2916. kinetics and thermodynamics of uranium by Citrobacter freudii. J. Environ.
Rui, X., Kwon, M.J., O'Loughlin, E.J., Dunham-Cheatham, S., Fein, J.B., Bunker, B., Radioact. 99 (1), 126e133.
et al., 2013. Bioreduction of hydrogen uranyl phosphate: mechanisms and U (IV) Xu, Y., Zhou, N.-Y., 2017. Microbial remediation of aromatics-contaminated soil.
products. Environ. Sci. Technol. 47 (11), 5668e5678. Front. Environ. Sci. Eng. 11 (2), 1.
Sahay, V., Mude, S., Samant, B., 2015. The Early Eocene Naredi Cliff Section, Kutch Yan, X., Luo, X., 2015. Radionuclides distribution, properties, and microbial diversity
Basin, Gujarat, India: Evidences of a Condensed Stratigraphic Section. of soils in uranium mill tailings from southeastern China. J. Environ. Radioact.
Sasaki, K., Takeno, K., Shinkawa, H., Sasaki, K., Das, N., 2015. Removal of radioactivity 139, 85e90.
and recovery of radioactive Cs from sediment mud and soil in Fukushima, Japan Yin, Y., Wang, J., Yang, X., Li, W., 2017. Removal of strontium ions by immobilized
using immobilized photosynthetic bacteria. In: Advanced Materials Research, Saccharomyces cerevisiae in magnetic chitosan microspheres. Nucl. Eng.
vol. 1091. Trans Tech Publications, pp. 125e130. Technol. 49 (1), 172e177.
Shaowei, W., Zhaorong, S., Ping, W., Guoliang, W., Yuqin, D., 2017. Study on