Journal of Environmental Radioactivity 180 (2017) 27e35

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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: drarpitshukla@gmail.com (A. Shukla), sarafmeenu@gmail.com
(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
Microorganisms, being the witness and survivor of various
extreme conditions on Earth over the time, are today been
exploited in remediation of radioactive waste. They possess the
advantage of being environment friendly, easy to grow, adapt-
ability, specificity, ability to carry out desirable reactions and
processes-with generation of no or minimal polluting byproducts.
They possess the characteristic self-sustaining capability (Gazso
,
2001). This review provides an insight into the occurrence of mi-
crobes in environments containing radionuclides, the mechanisms
involved for its survival and tolerance to radiation with special
emphasis on the interactions between the bacterial cell and ra-
dionuclides which show immense potential for bioremediation.
The use of bacteria in bioremediation of radionuclides is also briefly
discussed later in this review.
2. Radiation and microorganisms: exposure and survival
2.1. Effect of ionizing radiations
It is important to acknowledge the lethal implications of
radioactive substances. Gamma rays and other ionizing radiations,
in general, have been known to inhibit reproduction of microbes by
engaging in alteration of DNA (IAEA, 2017). The detrimental effects
of ionizing radiations occur on the core nuclear material of any cell-
the DNA. Exposure to such stress could lead to formation of lesions
leading degradation of DNA by direct and indirect mechanisms.
Directly, an electron is ejected out of the DNA whereas indirect
pathway involved the process of radiolysis (Ravanat and Douki,
2016).
2.2. Mechanism of resistance and/or tolerance to ioning radiations
The most radioresistant bacteria, Deinococcus radiodurans has
been studied extensively. Lethal dose (LD10) for D. radiodurans R1
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
species of Chroococcidiopsis have been reported to survive up to
15
103 Sv and with members of genus Micrococcus exhibiting a
more humble radiation resistance (Brim et al., 2000; Krabbenhoft
et al., 1965). Radionuclide 241Am imparted a chronic effect on the
growth of Photobacterium phosphoreum, a bioluminescent bacte-
rium, with a decrease in its growth while increasing the intensity
and duration of its luminescence at low temperatures. Alexandrova
et al. (2011) attributed it to the formation of peroxides in the me-
dium solution resulting from radiolysis of water. The same study
also noted the accumulation of 241Am in DNA of the bacterium. In
addition to radiation, the bacteria have also exhibited resistance to
desiccation, ultraviolet radiation and oxidative agents. While
investigating the cause of such immense resistance, the presence of
multiple pathways for amino acid synthesis have been identified
(Venkateswaran et al., 2000). It was found that accumulation of Mn
(II) in the bacterium promoted resistance (Daly et al., 2004). The
genetic basis for radiation resistance in the bacterium was found to
be an exonuclease repair pathway, as investigated by Misra et al.
(2006). Deinococcus radiodurans was been found to survive
ionizing radiation levels up to 10
103 Sv (Cox and Battista, 2005).
U, Ni, Co, Cu and Cd resistant bacteria belonging to the genus Ba-
cillus, Serratia and Arthrobacter, Pseudomonas, Rhodococcus, Bacillus
were been discovered. Upon subjected to further studies, resistance
was revealed to be due to instrinsic characteristics of the bacteria.
Intracellular sequestration of U was found to contribute to resis-
tance while processes such bioprecipitation and biomineralization
were found to limit the toxic effects of U. (Choudhary et al., 2012;
Merroun and Selenska-Pobell, 2008; Choudhary and Sar, 2011;
Suzuki and Banfield, 2004). Bioadsorption and ‘localized biomin-
eralization’ have shown to be responsible for providing uranium
resistance to Pseudomonas aeruginosa J007 and Arthrobacter nic-
otianae (Suzuki and Banfield, 2004). It was recently discovered a
unique interaction between bacteria, isolated from spent nuclear
fuel pond, and Co2þ. It showed that the tolerance to cobalt was due
to an efficient efflux pump mechanism similar to that of Ni2þ and
Zn2þ -since cobalt tolerance is usually associated with them
(Dekker et al., 2014). Members of genera Serratia are known to be
resistant to Cs137, Sr90 and Co60 (Paterson-Beedle et al., 2006).
Resistance to nickel and cobalt in E. coli has been acknowledged to
the presence of a novel YohM protein rcnA, a first that does not rely
on the traditional NiCoT (Nickel Cobal Transporter) family
(Rodrigue et al., 2005). S-layer proteins have also been identified to
provide resistance against gamma-radiation (Gerbino et al., 2015).
The studies following the devastating accident in Chernobyl
revealed that radiation from nuclear power plant had a positive
effect on in spore germination in areas, affected by radiation. The
phenomena was later termed as ‘radiostimulation’ (Dadachova and
Casadevall, 2008). In the same study, Chernobyl-associated fungi
exhibited radiotropism and exhibited their ability to utilize radia-
tion as source of energy.
3. Soil and microorganisms
3.1. Soil as habitat
Soil serves as one of the most important habitats. Teeming with
variety of nutrients, organic matter and even metals soil serves as
one of the most economical ecosystems for the growth and pro-
liferation of microbes. From species (taxonomic) to functional and
from proteomic to genomic, soil continues to swell the already
exhausting list of microbes. As previously mentioned, microbes
have even been isolated from soils containing radionuclides.
3.2. Radionuclides in soil
Radionuclides are usually been dispersed in nature, in minute
concentrations. Natural radioactivity results primarily due to 4 K
and from the members of 238U decay chain. Incidence of U, Rn, Th in
agricultural lands of Bulgaria and Cu, Cd and Pb from acid drainage
waters have instigated the development of various bioremediation
techniques for radionuclide pollutants (Groudev et al., 2001).
Following the applications of Rhodococcus, Nocardia and Dein-
ococcus radiodurans in remediation of radwaste with concentra-
tions greater than 10 mCi of 137Csg1 and for concentrations greater
than 20 mCi 137Csg1 respectively, model microbes Deinococcus
radiodurans, Pseudomonas putida, Shewanella putrefaciens CN32
have been reported to be used as pure culture in remediation (Lloyd
and Renshaw, 2005). Commercial acid-leaching of radionuclides
from mine has been one of the prime causes of terrestrial presence
of radionuclides (U, Th, Pu) and some heavy metals (Cu, Cd, Pb) in
agricultural lands in Bulgaria (Groudev et al., 2001). A recent study
devised an expedient method for identification and estimation of
concentration of naturally occurring radioactive material (NORM)
in soil horizons (Michalik, 2017). It has been duly emphasized upon
that, chronic radiation in an oligotrophic environment leads to
excersion of selective pressure to enhance certain microbes which
significantly alters the richness, diversity and abundance of bacteria
in that environment (Tisa
kova
et al., 2013). In India, naturally
occurring radionuclides are; 238U, 232Th, 4 K, 226Ra, Ca. Levels of
radiation in South Konkan village soil are 68.08
109 Svh1.
 A. Shukla et al. / Journal of Environmental Radioactivity 180 (2017) 27e35
Responsible radionuclides are 238U, 232Th, 4 K (Dhawal et al., 2013).
In the South Indian coastal state of Karnataka radionuclides 232Th,
4
K, 226Ra account for 74
109 Svh1 (Narayana et al., 2001).
Presence of 238U, 232Th, 4 K in another coastal South Indian state of
Tamil Nadu has also been described (Ravisankar et al., 2012). In the
western state of Gujarat, occurrence of radioisotopes of Th and Ca
from Naredi Cliff and, U and Th in the groundwater of Thar Desert
respectively, has been reported (Sahay et al., 2015). In the north-
eastern Indian state of Jharkhand, uranium mining and milling
from Jaduguda uranium mine into the Bay of Bengal have been
found to be emitting alpha particles that has affected the local
microbial communities (Dhal and Sar, 2014).
3.3. Interactions between bacteria and radionuclides
It is due to the presence of soil-dwelling microbes that the
biogeochemical cycling of N, C, S, P and Fe occur (Prescott et al.,
2006). Nevertheless, before commencing the process of biogeo-
chemical cycling of compounds, microbes must first interact with
them. Such processes take place only after successful interactions
between the microbial cell and the nuclide. To study such in-
teractions, a remarkable notion of bioavailability and bio-
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-
clide activity adsorbed by a solid phase to the concentration of
radionuclides absorbed in the aqueous phase, as Bq kg1 soil
(Tamponnet et al., 2008; Sheppard et al., 2009). For this review, it is
imperative to consider the role of bioavailability of radionuclides in
soil. Haferburg and Kothe (2007), discussed presence of noxious
contaminants in biotopes. They attributed bioavailability to be
reliant on the constitution of soil matrix, climatic conditions, mi-
crobial activity and water flow. Fig. 1 summarizes various mecha-
nisms of interactions found in bacteria. In soil, radionuclide cations
are less mobile (Shaowei et al., 2017). A detailed investigation of
Fig. 1. Various interaction mechanisms between microorganisms and radionuclides.
29
various factors affecting interactions between microbes and ra-
dionuclides in soil had been carried out and stated in the 5th Eu-
ropean Framework Program: BORIS. It primarily focused on the
bioavailability of Cs, Sr and Tc in soil (Tamponnet et al., 2008).
Often, the mechanisms involved in interaction between radionu-
clide and microbe also include metals (Tabak et al., 2005; Van
Hullebusch et al., 2005). Uranium, one of the most crucial radio-
nuclides with wide applications, exists in soil in the oxidation states
of U(IV) and U(VI). Both are soluble in water and their migration is
heavily dependent on pH, ligand concentrations and redox status
(Krupka et al., 1999). A list of indigenous bacteria isolated from
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-
tion in removal of radionuclides from environment (Tisa
kova

et al.,
2013). Bacteria interact with radionuclides in various ways, as
enlisted in Table 2. It is interesting to note that, the actual mecha-
nisms of interaction of bacteria with radionuclides is in many ways
similar to those of heavy metals. Various sub-interactions have also
been listed in the table however, they work on the fundamental
principles of biotransformation, biosorption, bioaccumulation,
bioprecipitation and biosolubilisation. These five principles are
described in detail.
3.3.1. Bioaccumulation
Bioaccumulation is the “retention and concentration of a sub-
stance within an organism” (Tabak et al., 2005). Jorgensen (2010)
summarized bioaccumulation as “an enrichment of contaminants
in organisms relative to that environment.” The phenomena of bio-
concentration and biomagnification comprise bioaccumulation. It
relies on adsorption of radionuclides on to the cell surface due to
electrostatic attraction forces existing between the metal cations
and the negatively charged cell surface, resulting in an electrostatic
binding. Staunton et al. (2002) found a decrease in distribution
coefficient of radiocaesium with an increase in organic matter in
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-
accumulation process can be either active or passive. Active bio-
accumulation is a relatively slower process, requires more energy
and can be dependent or independent of metabolism. Passive
bioaccumulation had been found to be more favorable in areas with
nutrient limitation. It is also faster and less energy consuming than
active process. (Haferburg and Kothe, 2007). Accumulation could
be either intracellular or extracellular. Intracellular accumulation of
radionuclides could be attributed directly to the presence or
absence of the respective radionuclide transporter, effect of nuclide
on permeability of the cell membrane. (Merroun and Selenska-
Pobell, 2008). A study by Francis et al. (2004) showed that intra-
cellular accumulation of U(VI) in Citrobacter sp. and Halomonas sp.
was largely in form of phosphates such as; hydroxophosphate or
polyphosphates or as uranium hydrogen phosphate. Accumulation
of iodide on soil Bacillus subtilis cell wall were found to intensify up
on addition of glucose. (Amachi et al., 2005). Bacillus vallismortis
showed to bioaccumulate U(VI) at 5 mg/L concentration after 72 h
of inoculation. About 50 mg/g (metal/dry bacteria) U(VI) was
accumulated which was later determined by UVeVis spectropho-
tometry (Ozdemir et al., 2017). An interesting research on radio-
nuclide exchange between uranium and a proton was determined
using a separation factor and it was revealed that, members of
Gram-positive bacteria namely, Micrococcus luteus, B. subtilis and
B. megatarium showed potential for accumulation of Th in a solu-
tion containing Th and U. (Tsuruta, 2006).
Since bioaccumulation involves rapid interactions with anionic
groups present in components of cell surface, it is significantly
affected by molecular properties of the nuclide, properties and
characteristics of the bacteria present (Tisa

kova

et al., 2013). Size
and lipid content also influences it, with a decrease in size leading
to less surface area for accumulation. (Jorgensen, 2010). Presence of
capsule or slime or S-layers dramatically influences the bio-
accumulation process. Once accumulated, the nuclides are being
acted up on by polyphosphate bodies. Such intracellular chelation
mechanisms have suggested to give rise to metal and subsequent
radionuclide tolerance (Keasling and Hupf, 1996). However, Jiang
et al. (2004) stated that, it is the surface characteristics of the
bacterial cell wall-which determines its adsorption properties. The
differences in cell wall composition in Gram-positive and Gram-
negative bacteria showed little to no significance on bio-
accumulation capability.
3.3.2. Biosorption
Prakash et al. (2013) described the phenomenon of biosorption
as, “the sequestration of positively charged metal ions to the negatively
charged cell membranes and polysaccharides secreted on the outer
surfaces of bacteria”. Bacterial cell wall comprise peptidoglycan or
lipopolysaccharide, for Gram positive and Gram-negative bacteria
respectively. However, owing to the phosphate moiety there exists
an electronegative membrane charge to which positive cations of
metals and radionuclides are attracted. Such attraction force leads
to adsorption of the nuclides on to the surface of the cell. Bio-
sorption can occur directly, by interaction of nuclide cation with
anionic cell wall functional groups or it could be indirect, with
either EPS, S-layer or capsule. Since the binding of nuclides with cell
wall could also be due to ligands such as, carboxyl, amine, hydroxyl,
phosphate etc., it is described as a passive uptake process (Merroun
 A. Shukla et al. / Journal of Environmental Radioactivity 180 (2017) 27e35
and Selenska-Pobell, 2008 and Luk'yanova et al., 2008). Bacterial
strains capable of accumulating 60Co, 89Sr, 106Ru, 131I, 135Cs and
144
Ce had been acknowledged with the help of autoradiography
technique (Kokke et al., 1969). Extracellular polymeric substance
(EPS) obtained from Rhodococcus opacus and R. rhodochrous had
been used as sorbents for the sorption of Cd(II), Pb(II), Ni(II), Co(II)
and Cr(VI) ions. Biosorption leads to immobilization of the radio-
nuclide. The process is species specific and, is influenced by tem-
perature, aeration, pH, phase of growth of cells, secretion or
production of exopolymers; presence of organic or inorganic con-
tent and metabolites. Electrostatic attraction, chemical interaction
of extracellular biopolymers and functional groups as well as metal
ions also influence biosorption (Dobrowolski et al., 2017). Xie et al.
(2008) observed in their study, that carboxyl present in cell wall of
Citrobacter freudii served as one of the active sites for biosorption
and exhibited significant effect on sorption. They concluded that
since dead cells exhibit better sorption ability, the entire process
was influence by the presence of functional groups in cell wall than
any other biological activity of the cell. The biggest shortcomings of
biosorption are; quick saturation with nuclide molecules and
competitive desorption occurring due to cations, other than the
desired one, for binding site on to the cell (Jabbar and Wallner,
2015). Hence, biosorption is generally applied for removal of low
concentration radionuclides from effluents (Merroun and Selenska-
Pobell, 2008).
3.3.3. Biotransformation
Bioavailability and concentration of radionuclides can be
dramatically altered by bacterial processes (Francis, 2007). Redox
reactions lead to a change in solubility of the nuclides, pH revises
their solubility (Francis and Nancharaiah, 2015). Thus, key chemical
processes by bacterial transformations lead to formation of oxides,
coprecipitates, ionic, organic or inorganic complexes of radionu-
clides (Francis and Dodge. 2009). Both, the aerobic and anaerobic
bacteria that are actively growing, possess the ability of biotrans-
formation via redox reactions. Usually, non-sorptive nuclides are
either transformed enzymatically or non-enzymatically. Microbes
possess the ability to utilize oxidised form of radionuclides and
metals such as U, Tc, Cr as terminal electron acceptor (TEA). Oxi-
dised form of such nuclides are water-soluble and mobile while
their reduction results in their precipitatation. Soluble forms of U,
Tc and Cr are U(VI), Tc(VIII) and Cr(VI) respectively (Tabak et al.,
2005; Lovley, 2002). The reported bacteria and archaea that
dominate biotransformation reactions are those capable of
dissimilatory Fe(II) or sulphate-reducing bacteria (DIRB and DSRB),
for example, Geobacter sulfurreducens strain PCA and Anaeromyx-
obacter dehalogenans strain K and Shewanella putrefaciencs strain
CN-32. Bioreduction and bioprecipitation ultimately results in
immobilization of the radionuclide (O'Loughlin et al., 2011; Rui
et al., 2013). Role of triheme periplasmic cytochrome type-c had
been identified to be a crucial for biotransformation (Jabbar and
Wallner, 2015). Differences in direct and indirect bacterial reduc-
tion of radionuclides is depicted in Figs. 2 and 3.
Enzymatic reduction of metals and radionuclides has been
extensively observed in bacteria such as; Shewanella oneidensis, S.
putrefacriens, Geobacter metallireducens. Reduction of Tc has been
reported under varying pH conditions, parallel to formation of H2O
during metabolism (Jabbar and Wallner, 2015). Anaerobic reductive
dissolution of Pu(IV)-Pu(III) by Bacillus sp., S. marcescens, Clos-
tridium sp. has been reported by (Francis, 2007). A highly non-
sorptive radionuclide Np(V) undergoes anaerobic bioreduction
and biomineralization processes in presence of either hydrogen,
pyruvate or citrate (Rittmann et al., 2002; Mohapatra et al., 2010).
Desulfovibrio desulfuricans has been reported by Icopini et al. (2007)
to successfully carry out reduction of Np(V). In dissimilatory
31
reduction of radionuclides, the reduction of radionuclide is con-
current to energy metabolism. It includes use of a substance as an
electron acceptor for generation of energy. The electron acceptor is
reduced but not incorporated into an organic matter during the
biosynthetic anabolism process (Lloyd and Lovley, 2001). The
biggest bottleneck of this process is that it is, exclusive to obligate
anaerobes. (Gadd, 1996). Addition of riboflavin has proven to
enhance microbial reduction rates of Tc(VI), Np(V) and Pu(IV) by
Shewanella oneidensis (Cherkouk et al., 2016). The same study
concluded that riboflavins could be very well be used to signifi-
cantly accelerate the process of bioremediation of radionuclide
containing waste.
3.3.4. Biosolubilisation
Biosolubilisation is a result of autotrophic metabolism during
which, radionuclides are leached out from their solid matrices
(Gadd, 2002). It is an indirect method of solubilisation as the
autotrophic bacteria obtain energy from reduced Fe or S com-
pounds whilst solubilizing the nuclides and metals. It requires
acidic pH, moisture and oxygen to oxidise Fe, S and leach out metals
as sulfides. Such bacteria are mesophilic and acidophilic in nature
(Ghauri and Johnson, 1991). Usually, a mixture of acid and bacteria
along with an inorganic source of energy is added to mines of
metals and radionuclides, after the application of physical, chemical
and other hydrometallurgical process for solubilisation (Pandey
and Natarajan, 2015). Acidithiobacillus ferrooxidans, Aciditiobacillus
thiooxidans, Leptospirillum ferrooxidans, Sulfolobus (Ewart and
Hughes, 1991; Bosecker, 1997; Munoz et al., 1995) have been re-
ported to solubilse metals.
It is affected by the oxidation state of the nuclide, pH sur-
rounding the bacteria, moisture and inorganic content as substrate
for the bacteria. Presence of citrate, a crucial bacterial metabolite,
leads to an increase in solubility of nuclides for an extended period
of time. However, uranyl citrate complex dissociates in conditions
with greater salinity and presence of phosphate-leading to pre-
cipitation of uranium and citric acid. Thus, citric acid acts as a
crucial effector in the process of biosolubilisation (Francis et al.,
1992).
3.3.5. Bioprecipitation
Precipitation results after successful conversion of soluble form
of a nuclide into its insoluble form. In case of radionuclides, as
mentioned above, their reduced forms are highly insoluble-
resulting in their precipitation. Precipitation of metals and radio-
nuclides occur mostly as carbonates or hydroxides. The importance
of oxidation state and valence of the radionuclide in bio-
precipitation remains undisputed. The site of precipitation on mi-
crobial cell is known as the ‘nucleation site’ and it depends on the
concentration of ligand produced by the cell. Microbially produced
ligands and biogenic formation of minerals influence precipitation
of the radionuclide (Jabbar and Wallner, 2015). Bacterial secretions
and metabolism can lead to a localized change in pH, Eh in its
surrounding thus, also changing the pH of the immediate vicinity of
the metal. (Merroun and Selenska-Pobell, 2008). Co-precipitation is
another interesting phenomenon where elements are amalgam-
ated in metal oxide minerals during their precipitation (Tabak et al.,
2005).
3.3.6. Miscellaneous
3.3.6.1. Chelation. Microbial production of chelating biopolymers,
such as pyomelanin, melanin etc. have shown to modify the
mobilization of radionuclides significantly (Tamponnet et al.,
2008). Exposure of such melanin to ionizing radiation has also
demonstrated an increase in growth and biomass in fungi; Cryp-
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
byproducts, such as siderophores, have been widely studied on
pseudomonads (Meyer, 2000). reported production of a fluorescent
siderophore pyoverdin by P. grimontii. However, siderophore pro-
duction exhibiting considerable sorption capacity, by P. fluorescens
and P. stutzerii in presence of radionuclides 147Pm, 234Th and 241Am
was studied by Arlinger et al. (2003). Such studies shed light on
mobilization of radionuclides in groundwater.
3.3.6.2. Complexation. Complexation results when organic phos-
phate groups and teichoic acid and radionuclides interact with each
other. U(VI), for example, can be complexed on to the cell wall of
Gram-positive bacteria since they are relatively rich in teichoic acid
content, in contrast to Gram-negative bacteria. Gadd (2002) states
the complexation of Co2þ by citric acid, a bacterial metabolite.
Nutrient transporter-analogue of K was reported to transport Cs137
into the cell (Shaw, 2005; Bennett and Willey, 2003). Speciation
and binding of radionuclides to fungal cells influences its precipi-
tation capabilities. Thus, retention of Cs in forest soil had been
accredited to mobilization, uptake and translocation of radionu-
clides and nutrient by fungi (Steiner et al., 2002). Sequestration of
Sr in Serattia sp. produced hydroxyapatite was reported by
(Handley-Sidhu et al., 2011a,b). Complexing agents include
ethylene diamine tetra acetate (EDTA), diethylene triamine penta
acetic acid (DTPA), oxalate, citrate, humic acid, fulvic acids, bi-
carbonates etc. (Luo and Gu, 2011; Wan et al., 2008).
4. Microbial remediation of radionuclides
Exposure to radionuclides is a health as well as an
ecotoxicological concern. Microbes possess an immense potential
for undergoing sustainable manipulations for biotechnological
applications. It is hence palpable to use microbes in removal of
radionuclides from environment. Some typical processes involved
have been summarized in Table 3. Natural attenuation involves on
the intrinsic bioremediation potential without any human inter-
vention and-being recalcitrant and persisting in nature, radionu-
clides have been the cause of concern for the scientific community
(Francis and Nancharaiah, 2015). Ultimately, it were the indigenous
bacteria that rose to the occasion and have since been subjected to
extreme scrutiny for their potential biotechnological application.
Radionuclides cannot be destroyed but can only be transformed.
The ones with greater solubility can be immolibilized while those
with lesser solubility can be flushed out. A change in immediate
vicinity of the radionuclide can aide in modifying the solubility of
radionuclides (Hazen and Tabak, 2005). Turick and Berry (2016)
reviewed microbial activity involved in degradation of concrete
where, nuclear waste was bring stored. A comprehensive compi-
lation of database of bacteria and fungi, wild type or recombinant,
which are been used in remediation of radioactive waste, has been
created as ‘BioRadBase’ (Reena et al., 2012). Xu and Zhou (2017)
enlists the significant advantages in using microbes for remedia-
tion of radioactive waste are:
(a) High specificity
(b) High reusability
(c) High efficiency
(d) Complete removal of pollutant
(e) Low expense
(f) No secondary pollution
 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
microbial activity, to a sample is called bioaugmentation (Xu and
Zhou, 2017). The application of microorganisms in bioremediation
of radionuclides is limited to their ability to tolerate, survive and
resist high levels of radiation while simultaneously carrying out the
desired function (Brim et al., 2000). In situ approach of bioreme-
diation in marine sediments have been discussed by Lofrano et al.
(2016). In bioremediation; bioaugmentation, biostimulation, bio-
mineralization and dissimilatory reduction have been extensively
used (Hazen and Tabak, 2005; Lloyd and Lovley, 2001). It has been
noted that immobilization and precipitation play a significant role
in remediation of metal and radionuclide contaminated sites (Islam
and Sar, 2011). Development of a ‘bio-inorganic ion exchanger’ has
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
et al. (2006). The experiment made us of immobilized biofilm of
Serratia sp. coated with hydrogen uranyl phosphate. Removal of
radionuclides was facilitated by intercalation of target species onto
a polyurethane foam matrix. Hence, the mechanism of removal
relied on the fundamental principles of cation exchange intercala-
tion. Immobilized arginate beads containing photosynthetic bac-
teria Rhodobacter sphaeroides showed to remove 59e74% Cs from
soil as well as sediment mud. The advantage of the method was
that, the beads could be easily recovered and reused without any
prominent loss of efficiency (Sasaki et al., 2015). Mumtaz et al.
(2013) carried out an interesting study which concluded the
growth of fungi subjugates bacteria in presence of high concen-
trations of radionuclides.
Regardless of the processes or mechanisms involved, bacteria
have established themselves as an alternative to the conventional
techniques of radiation and heavy metal nuclide remediation. It is a
matter of time when their true potential is recognized and the first
step in achieving their potential is knowing their varying ways of
interaction with them.
5. Challenges and future prospects
There exists no reservations that microbes, specifically bacteria
and archaea, possess tremendous knack to not only withstand
extreme conditions but also carry out important biotechnological
processes. Contrary to their microscopic size, they have relentlessly
shown to carry out certain vital and unique processes without
which other life might not be able to sustain or even exist. The
microbes have shown their ability to undergo genetic manipula-
tions and carry out their recombinant phenotypic traits. It is also
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
those of metals. Recently, the biotechnological applications of re-
combinant bacteria have shown encouraging results in remediation
of radwaste. It seems only prudent to make use of those microbes
that are indigenous to radionuclide containing natural samples,
such as soil, air or water, and subject them to extreme scrutiny for
exploring their capabilities. True potential of these microbial pro-
cesses can be unlocked by frequent and sustaining collaborations
with various fields of science and technology and, once character-
ized completely; these microscopic beings can be used, in isolation
or as a consortia, for removal of high concentrations of radwaste.
The removed radionuclide can be further used as substrate for
other commercial applications. The beauty of using microbes for
the job lies in their reusability. Such an approach could lead to the
development of an eco-friendly way for treatment as well as
extraction and/or recovery of precious radionuclides.
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