review article on the topic of biosorption of heavy metals

1. BIOSORPTION OF HEAVY METALS
Parvathy A1, Najiya P K2, Lekshmi J S3, Sahil Babu4, Rubeena S*
(1,2,3,4) Department of Biotechnology and Biochemical engineering, Sree Chitra Thirunal College
of Engineering, Pappanomcode Trivandrum Kerala.
*Assistant professor, Department of Biotechnology and Biochemical engineering, Sree Chitra
Thirunal College of Engineering, Pappanomcode Trivandrum Kerala.
Abstract
Our environment is highly degraded by the discharge of toxic heavy metals into aquatic systems,
as a result of various industrial operations. Humans, being at the top of the food chain are more
prone and vulnerable to heavy metal toxication. Ion exchange, solvent extraction, evaporation
reverse osmosis etc., are the traditional methods used to remove unwanted heavy metals from
waste water which is more tedious and expensive. Biosorption is a new and economical alternative
for removing toxic heavy metals from industrial waste water. Biosorption involves the selective
sequestering of metal soluble species which result in immobilization of metals by microbial cells.
Microorganisms such as bacteria, fungi, yeast, algae etc. are used as biomaterials for the removal
toxic metals. This physiochemical process can remove harmful metals like arsenic, lead cadmium,
cobalt, chromium etc. It may be used as environmental friendly filtering technique. The process
results in metal free effluents and small volumes of solution containing concentrated metals which
can be easily recovered. This review briefly describes the Biosorption process, mechanism, various
biosorbents used for heavy metals remediation from waste stream etc.
Keywords: Biosorption, Heavy metal, Biosorbents, Algae, Fungus, Bacteria, Biomass,
remediation.
Introduction
Our environment is highly degraded by the presence of toxic heavy metals. We humans, being at
the top of the food chain, are more prone and vulnerable to heavy metal toxication. Many methods
like metal ion exchange method, evaporation and extractions are used to remove unwanted heavy
metals from liquid wastewater, which is more tedious and expensive. Here comes the need to
directly sorb the heavy metals from the wastewater so that it eliminates the need to adapt the
inefficient and costlier processes.

2. The tedious process can be replaced by a physiochemical process termed as Biosorption which
involves selective sequestering of metal soluble species which result in the immobilization of
microbial cells. Algae and Saccharomyces cerivicea were used to remove heavy metals like lead
and copper from drinking water and an aqueous solution respectively. Biosorption by inactive
microbial biomass is more effective in removing high concentrations of toxic heavy metals from
aqueous solution.
The major source of biomass which is efficient as well as cheap is waste microbial biomass and
algae. Microorganisms like fungi and bacteria are also used. The complexity of microorganism’s
structure implies that there are various methods to carry out the process of biosorption which
includes metabolism dependent, non-metabolism dependent, extracellular, cell surface sorption,
intracellular accumulation. Biosorbents like multi metal binding biosorbents, made from a
combination of tea wastes, maple leaves and mandarin peels, were evaluated to study their
efficiency in absorbing heavy metals from the multi metal aqueous solution. Stability of
microorganism to withstand different environmental conditions and their ability to take up
pollutants and heavy metals as nutrients due to absorptive capability, made them suitable for using
as a biosorbent. [1-8] Some of the heavy metals, their major sources, their toxic effects in human
and threshold limit values are given in the Table 1
Table 1: types of heavy metals, their source and toxic effect.
Heavy
metals
Major source Toxic effect Threshold
limit value
(mg/m3)
Reference
Arsenic Pesticides, fungicides, metal smelters Bronchitis, dermatitis and
poisoning
0.5 [9]
Cadmium Welding electroplating, pesticide
fertilizer, nuclear fission plant, Cd and
Ni batteries
Renal dysfunction, lung
disease
0.2 [9]
Lead Paint, pesticide, smoking, automobile
emission, mining, burning of coal
Mental retardation in
children, damage to
nervous system
0.2 [9]
Manganese Welding, fuel addition,
ferromanganese production
Damages to central nervous
system.
5 [9]
Chromium Mines, mineral sources Damage to nervous system,
fatigue, irritability
1 [9]
Zinc Refineries, brass manufacture, metal
plating, plumbing
Corrosive effect on skin 5 [9]
Copper Mining, pesticide production,chemical
industry, metal piping
Anemia, liver and kidney
damage
1 [9]
Mercury Pesticides, batteries and paper industry Tremors, gingivitis and
protoplasmpoisoning
0.01 [9]

3. This review aims at giving insight to the advantages of biosorption and their mechanism. This
review also discusses about the factor which affects the biosorption process. Some of the algae,
fungi and bacteria and their biosorption process are discussed for more understanding.
Advantages of Biosorption
Advantage of biosorption are given below:
i. Growth-independent, non-living biomass is not subjected to toxicity limitation of cells.
No requirement of costly nutrients required for the growth of cells in feed solutions.
Therefore, the problems of disposal of surplus nutrients or metabolic products are not
present.
ii. Biomass can be procured from the existing fermentation industries, which is essentially
a waste after fermentation.
iii. The process is not governed by the physiological constraint of living microbial cells.
iv. Because of non-living biomass behave as an ion exchanger; the process is very rapid
and takes place between few minutes to few hours. Metal loading on biomass is often
very high, leading to very efficient metal uptake.
v. Because cells are non-living, processing conditions are not restricted to those
conducive for the growth of cells. In other words, a wider range of operating conditions
such as pH, temperature and metal concentration is possible.
vi. No aseptic conditions are required for this process [3].
Biosorption Mechanism
Understanding the mechanism of metal uptake by microorganisms is an essential step, as it would
help in analyzing the concentration of microbial biomass, removal and extraction [3]. To reduce
heavy metal pollution several methods like adsorption, precipitation, ion exchange, electro dialysis
and reverse osmosis are used. Depending upon the cell structure many ways can be adapted to
capture the metal. They can be divided on the basis of their cell metabolism as metabolism
dependent and non-metabolism dependent. On basis of the location where the metal is removed
mechanisms can be categorized as extracellular and intracellular accumulation, and cell surface
sorption [2]. Metabolism independent uptake of metal simply involves the metal binding to the
cell wall and an external surface is the only mechanism present in non-living biomass Metabolism-
dependent uptake essentially involves adsorption process such as ionic, chemical and physical
adsorption. A variety of ligands located on the fungal walls are known to be involved in metal
chelation. Metal ions could be adsorbed by complexing with negatively charged reaction sites on
the cell surface [3]. Mechanism of biosorption process in shown in Figure 1.

4. Figure 1 Types of biosorption
The biosorption process involves a solid phase (sorbent) and a liquid phase (normally water) and
dissolved metal ions. Due to the higher affinity of the sorbent and sorbate the sorbate is usually
taken up by the sorbent and this process continues till an equilibrium is established between the
sorbent and sorbate [3]
The metal biosorption process involves a two-step process. In the first step metal ions are adsorbed
to the cell surface by interactions between metals and functional groups displayed on the cell
surface. All the metal ions before gaining access to cell the cell membrane and cell cytoplasm
come across the cell wall. The cell wall consists of variety of polysaccharides and proteins and
hence offers a number of active sites capable of binding metal ions [3].
Different group of microorganisms vary in their cell wall composition. Algal cell walls are mainly
cellulosic, where the potential metal binding groups are carboxylates amines, imidazole,
phosphates, sulfhydryl, sulfates and hydroxyls. Cell walls of bacteria are mainly composed of
peptidoglycan, which consists of linear chain of NAM and NAG. Fungal cell wall is made of chitin
In second step due to active biosorption metals penetrates into the cell wall.
Metal uptake by non-living cells is mainly by passive mode, which is devoid of energy and the
process take place through chemical composition of the cell wall. Studies of Ahluwalia and Goyal
indicates that the 2 step process which include, a passive process taking place immediately and an
active process that takes place slowly [3].

5. Factor Affecting Biosorption
The major factors that affect the process of biosorption are i) pH ii) Initial ion concentration iii)
biomass concentration iv) temperature. pH is the most important of all. It affects the overall process
of biosorption compared to all other parameters. From the studies of Hu xia Jing, its’ reported that
the maximum biosorption capacity of Cu2+ by immobilized spent substrate of fragrant mushroom
biomass was obtained at pH 5 with 10 mg/L of Cu2+ initial concentration [11]. Du et al reported
that the maximum amount of dye was adsorbed by heating of biomass significantly which in turn
increased the permeability of the cell wall so that dye could enter into the cells and be adsorbed to
intracellular proteins [12]. Biomass concentration is another factor that influences the metal
uptake. It was confirmed by the studies of Garcia et al. The presence of metal in the medium
allowed the tolerance at a level comparable with that observed in the isolation [13]. Hence these
factors should be taken into account during the study of biosorption process. Asku et al reported
that the process in independent of temperature in the range 25-30oC [14].
Algae as Biosorbent
Algae belonging to a multi applicable group, can contribute to important sectors. Their major use
is to produce a wide range of primary and secondary metabolites, which is applied to food,
pharmaceutical and cosmetic industries. Moreover, they have been suggested as potential
feedstock for bioenergy and biofuel production. Because of their large surface area and high
binding affinity they have been reported to effectively remove metals from waste water. There are
mainly two different types: Macro algae and Micro algae. Macro algae, especially brown algae,
have been found to be very effective biosorbents in removing heavy metals from wastewater
because of their high uptake capacities, similar to commercial ion-exchange resins and their
availability in nearly unlimited amounts from the ocean [15,16]
Laminaria japonica, brown algae were chemically modified by crosslinking with epichlorohydrin
(EC1 and EC2), or oxidizing by potassium permanganate (PC), or crosslinking with
glutaraldehyde (GA), or only washed by distilled water (DW). They were used for equilibrium
sorption uptake studies with Cd2+, Cu2+, Ni2+ and Zn2+. The experimental data proved that
maximum metal uptakes for Cd2+, Cu2+ and Zn2+ was EC1 >EC2 > PC >DW>GA, but the uptakes
of Ni2+ are almost the same for these sorbents [15]. The work of Anastopoulos et al discusses about
the alternative uses of algae (micro and macro) as biosorbents for water and waste water
decontamination [16].
Chlamydomonas reinhardtii exhibited the ability to biosorb and accumulate Cu and Pb, which was
shown by the studies of Flouty et al. He inferred that dead algal cells showed higher removal
efficiency than living cells and intracellular accumulation of metal ions seems to be limited by
living algal cells. Living cells had similar affinity for both metal ions. However, dead cells showed
a higher affinity for Pb (II) ions compared to Cu (II) ions [17]. Zhang et al studied on the
biosorption of phenanthrene on the field collected planktons and their fractions. His observation
helped in understanding the role of polarity, lipid and non-hydrolysable carbon fractions, and
aliphatic structures in the biosorption of Phen [18].

6. The dried filamentous green algae Oedogonium sp. the algal biomass obtained from the gold
mining sites were used for the sorption of heavy meals like Cu, Co, Cr, Fe, Hg, Ni, Zn and U in
singe and multi ion solutions by Bakatula et al [19]. In the studies of Zhenning Lou et al the raw
brown algae L. japonica was chemically modified by glutaraldehyde in order to reinforce it for the
sorption applications and also to enhance the sorption performance, which can fulfill the need of
cost effective and environmentally benign method for the fractional recovery of molybdenum and
rhenium from wastewater [20]. Ulothrix cylindricum, green algae were used in the characteristic
study of As(III) biosorption from aqueous solutions as a function of pH, biomass dosage, contact
time and temperature, which followed a pseudo second order kinetics [21]. Romera studied the
sorption capacity of six different algae (green, red and brown) in the recovery of cadmium, nickel,
zinc, copper and lead from aqueous solutions. The optimum sorption conditions were studied for
each monometallic system. The optimum pH was 6 for the recovery of Cd, Ni and Zn, and less
than 5 for Cu and Pb. The best results were obtained with the lowest biomass concentration used
(0.5 g/L) [22]. Alkaline treated algae from the oil waste industries were used in the removal
cadmium (II). This was studied under batch and column rectors providing optimum temperature
and initial biomass concentration [23]. Four brown macro-algae, Ascophyllum nodosum, Fucus
spiralis, Laminaria hyperborean and Pelvetia canaliculata, were investigated as natural cation
exchangers for the removal of transition metals from a petrochemical wastewater and concluded
an ion exchange equilibrium data for Cu, Ni, Zn and Ca. The equilibrium affinity constants for the
functional groups decreased in the following order: Cu > Zn > Ni • Ca, except for L. hyperborea,
which presents a lesser affinity for Ca [24].
Fungi as Biosorbent
Fungi are widely used in a variety of industrial fermentation processes which would serve as an
economical and constant supply source of biomass to remove metal ions from waste water. Fungi
can also easily grow in substantial amounts using unsophiscated fermentation techniques and
inexpensive growth media. Therefore, a fungal biomass could serve as an economical method for
removal or recovery of metal ions from aqueous solutions. [25]
Heavy metals like Hg2+, Cd2+ and Zn2+ from aqueous solution were biosorbed by Ca-alginate beads
and combining them with a white rot fungi Fungalia trogii biomass. The experiment was
conducted to study the enhancement and the adsorptive capacity of Ca-alginate beds. In this study
Ca-alginate beds were used as an adsorbent as well as a support material for the entrapment of
white rot fungus. The kinetics of Hg2+, Cd2+ and Zn2+ ions biosorption on the biosorbents depend
on the experimental conditions particularly medium, pH and metal ion concentration. The
biosorption capacity of the immobilized fungus was enhanced greatly when biosorption took place
following heat inactivation. Their results confirmed that alginate beads with immobilized cells can
be used in heavy metal adsorption studies without any detectable losses [26].
The work of Amany h et al evaluated the ability of the isolated fungal species from some
phosphatic fertilizers to remove uranium and some heavy toxic metals. He concluded that the five
fungal isolates were the efficient isolates for the growth in the liquid medium supplemented with

7. different heavy metals at high concentration (150 ppm). These isolates were later identified as
Aspergillus according to their morphological properties. [27]. Pleurotus eryngii has been proven
to be a promising alternative biosorbent for defluridation of water from real water samples to levels
below the WHO recommended value. The biosorption of fluoride on fungal biomass was observed
under pH2. Thermodynamic parameters revealed that the process of biosorption was spontaneous
and endothermic in nature [28]. Polyporous versocolor and Phanorochaete chrysoporium when
tested for different heavy metals varied in their results. P. versicolor displayed an adsorptive
capacity order of Pb(II) > Ni(II) > Cr(III) > Cd(Il) > Cu(II), whereas the order of P. chrysoporium
appeared as Pb(II) > Cr(III) > Cu(II) = Cd(Il) > Ni(II). Trametes versicolor mycelia were
immobilized using carboxyl methyl cellulose (cmc) as the natural polymeric matrix. After the
growth of the fungus on the matrix; live and heat inactivated forms were used for the biosorption
of Cu2+, Pb+ and Zn2+, from aqueous solution in a batch system [29].
Aspergillus fumigatus were used to study the biosorption of methylene blue. This study inferred
that dead fungal biomass can be used to treat industrial color effluents by biosorption. The process
is maximum when the initial concentration of methylene blue is 12mg/L, in an alkaline ph and
with an optimum temperature of 30oC [30]. Rhizopuscohnii is a filamentous fungus that have been
widely used in the modern industries for processing traditional fermented foods, industrial enzyme
production and organic acids production. The study inferred that this industrial fungus can be used
to remove cadmium in simulated waste water. The factors that affect he process includes the
biosorption capacity, such as pH the dosage and reusability of biosorbent and the initial cadmium
concentration was examined [31]
Bacteria as Biosorbent
The bacterial cell wall is the first effective compartment for adsorbing heavy metal particles
because it contains many anionic functional groups capable of binding to heavy metals, such as
peptidoglycan, teichoic acids, phospholipids and lipopolysaccharides. Microorganisms therefore
have a high potential for use in bioaccumulation and biosorption processes to remove heavy metals
from polluted environments [32].
Omar Chaalal et al developed a novel technique for the removal of strontium using two strains of
thermophilic bacteria, belonging to the Bacillus family [33]. Limcharoensuk et al investigated the
ability of three cadmium-and/or zinc-resistant bacteria, i.e. Tsukamurella paurometabola A155,
Pseudomonas aeruginosa B237, and Cupriavidus taiwanensis E324 in bioaccumulation and
biosorption of Cd2+ and Zn2+. The accumulations of Cd2+ and Zn2+ in cell walls and intracellular
spaces of these bacteria were compared [32]. The biosorption and biodegradation in the removal
process of 2, 2, 4, 4-tetrabromodiphenyl ether (BDE-47) by Pseudomonas stutzier KS0013 (Ps)
were investigated by S. Sun et al to elucidate the bio-dissipation mechanism with the influences
of glucose and rhamnolipids [34]. Inactivated form of three bacterial strains were investigated, i.e.
Actinomycete sp., Streptomyces sp. and Bacillus sp. for studying the capacity of bacterial biomass
to bind simultaneously with two metals cadmium and nickel [35]. Biosorption of each of the ions
Cd2+, Cu2+, Ni2+, Zn2+ and Mn2+ on Geobacillus toebii sub.sp. decanicus and Geobacillus
thermoleovorans sub.sp. stromboliensis in a batch stirred system was investigated by S. Ozdemir
et al [36].

8. Using lactic acid bacteria (LAB), H. Kinoshita et al tested the biosorption of heavy metals e.g.
cadmium (Cd)(II), lead (Pb) (II), arsenic (As) (III), and mercury (Hg) (II). Cd (II) in 103 strains
using atomic absorption spectrophotometery [37]. Utilizing different growth environments, this
study of Ryan Black developed a naturally occurring, heterogeneous mix of bacteria in suspended
and fixed morphologies. Both morphologies of bacteria were capable of adsorption and inferred
that fixed bacteria showed higher capacity and affinity for HMs removal [38]. Biosorption of
cadmium (II) ions from aqueous solutions by a glyphosate degrading bacterium, Ochrobactrum
sp. GDOS, was investigated in batch conditions by E. Khadivinia. The isolate was able to utilize
3 mm GP as the sole phosphorous source, favorable to bacterium growth and survival [39]. F.
Pagnaneli et al proposed an experimental and theoretical approach for the isolation and
quantification of mechanisms during heavy metal removal in batch reactors inoculated by sulphate
reducing bacteria in order to assess the real performance of the system and its duration in full-scale
realization [40]. Duck intestinal homogenate isolate Enterococcus faecalis DU10 produced
exopolysaccharide was characterized for its physicochemical, biosorption, antioxidant, antibiofilm
and rheological properties by P. Venkatesh et al [41].
Biosorption modelling
Biosorption equilibrium can be described by a number of available models in the literature. These
isotherms are characterized by definite parameters; their values express the surface properties and
affinity of biosorbent for different heavy metal ions. Three isotherm models i.e., Langmuir,
Freundlich and Temkin were used to analyze the equilibrium data in the study of Masoumeh
Akbari in his equilibrium and its kinetics and modeling of Cu(II) and Co(II).
The Langmuir model assumes a monolayer adsorption of solutes onto a surface comprised of a
finite number of identical sites with homogeneous biosorption energy, and can be expressed as
following equation:
qe = qmbLCe/(1+bLCe)
where qe is the metal uptake capacity (mg/g) and Ce is the equilibrium concentration of metal ions
in the solution (mg/L), qm is the biosorption capacity when the surface is completely covered with
metal ions (maximum biosorption capacity), and bL is a constant that represents the affinity
between the biosorbent and the metal ion.
The heterogeneity of the surface and multilayer biosorption to the binding sites located on the
surface of the biosorbent are considered in the Freundlich isotherm which is an empirical
expression and expressed as follows:
qe =kfCe
1/n
where kF is Freundlich constant indicating biosorbent capacity and n is Freundlich exponent
known as biosorbent intensity. The model parameters of Freundlich isotherm can be determined
from a plot of lnqe versus lnCe
The Temkin isotherm considering the effect of the biosorption heat that decreases with the
coverage of the biosorbent and the biosorbate–biosorbent interaction is given as:

9. qe = RTlnatCe/(bt)
where R is gas universal constant (8.314 J/mol K) and T is absolute temperature (K). A plot of qe
versus Ce enables the determination of the constant at and bt [42].
In Tau Wang’s “The numerical model of biosorption of Zn2þ and its application to the bio-electro
tower reactor (BETR)” study he considered a 2 D numerical kinetic model on the basis of flow
velocity and adsorption. This new model considers the adsorbed amount when equilibrium qe as
transient variable, which is superior to the old pseudo-first-order and the pseudo-second-order
model which regards qe as a constant. [43]
To identify the favorable adsorbents and adsorption process, Hall et al. introduced the following
dimensionless equilibrium parameter RL based on the Langmuir isotherm coefficient b;
RL = 1/(1+bC0)
This equation was used by Hall et al. and Chen and Wang to predict whether a sorption process
is favorable (0 < RL < 1), or unfavorable (RL > 1). The lower the value of RL is, the higher the
affinity of adsorbent to the adsorbed species., Pb2+ ions have lower RL values (0.061–0.537) than
Cu2+ ions (0.155–0.768) at similar environmental conditions; thus, yeast biomass has higher
affinity for Pb2+ ions. By increasing biomass dose in the biosorption tank from 0.75 g/l to 2.5 g/l,
RL values of Cu2+ ions slightly.
Conclusion
Biosorption is a useful and effective alternative against the conventional system. A set of cheap
and natural biosorbents with less or no toxic and side effects can be used to remove heavy metal
contaminated industrial effluents. Biosorption mechanism can be divided into two ways
- based on metabolism (dependent or non-dependent) or
- based on location where the metal is removed (extracellular and intracellular accumulation, and
cell surface sorption).
From the studies it is inferred that the microbial cells retain the activity in the Ph range of 6.This
will help in identifying the sorbent for biosorption process. Application aspects of biosorption are
aimed at biosorption process optimization. In this computational era, models are being developed
in transferring technologies from the lab scale to chemical process industries. For this, more
information on biosorption is essential to combine the best biomass, metal and with the
environmental conditions. Even though this is a cumbersome task, engineers are actively working
to develop a biosorption optimization.
Acknowledgement
I am extremely thankful to my college administration for providing an opportunity and my guide
miss. Rubeena S for her valuable guidance.

10. Reference
1. B Volesky, Biosorption for Industrial Applications.
2. F Veglio, Removal of Metal Ions by Biosorption.
3. S.S. Ahluwalia, D. Goyal / Bioresource Technology 98 (2007) 2243–2257.
4. S. Amirnia et al. / Chemical Engineering Journal 264 (2015) 863–872.
5. Y. Shang, X. Yu / Algal Research 12 (2015) 258–261.
6. V.K. Gupta et al. / Journal of Colloid and Interface Science 296 (2006) 59–63.
7. Advances in the biosorption of heavy metals, David Kratochvil and Bohumil Volesky.
8. A. Abdolali et al. / Science of the Total Environment 542 (2016) 603–611.
9. Heavy metals and living systems: An overview, Reena Singh.
10. Biosorption of heavy metals an overview, by Nilnjana
11. H. Xiao-jing et al. / Ecological Engineering 73 (2014) 509–513.
12. L.-N. Du et al. / Journal of Hazardous Materials 205– 206 (2012) 47– 54
13. García, R. et al.: Biosorption of Heavy Metal in aqueous solutions.
14. Asku Z, Sag Y, Kutsal T the biosorption of copper by C. vulgaris and ramigera, environ
technol.13 (1992) 579-586
15. F. Luo et al. / Chemosphere 64 (2006) 1122–1127
16. I. Anastopoulos, G.Z. Kyzas / Journal of Molecular Liquids xxx (2015) xxx–xxx.
17. R. Flouty, G. Estephane / Journal of Environmental Management 111 (2012) 106e114.
18. D. Zhang et al. / Chemosphere 93 (2013) 61–68
19. E.N. Bakatula et al. / Journal of Geochemical Exploration xxx (2014) xxx–xxx.
20. Z. Lou et al. / Chemical Engineering Journal 273 (2015) 231–239.
21. M. Tuzen et al. / Journal of Hazardous Materials 165 (2009) 566–572
22. E. Romera et al. / Bioresource Technology 98 (2007) 3344–3353.
23. D. Bulgariu, L. Bulgariu / Journal of Cleaner Production xxx (2015) 1e9.
24. Removal of Metal Ions from a Petrochemical Wastewater using Brown Macroalgae as
Natural Cation-Exchanger, by Maria A.P.
25. LUO Jin-ming, et al/Trans. Nonferrous Met. Soc. China 20(2010) 1104�1111
26. M. Yakup Arıca et al. / Journal of Hazardous Materials B109 (2004) 191–199.
27. Biosorption of uranium and heavy metals using some local fungi isolated from phosphatic
fertilizers, by Amany H.
28. F. Amin et al. / Environmental Nanotechnology, Monitoring & Management xxx (2015)
xxx–xxx
29. Heavy metal biosorption by white rot fungi, by Ulkii Yetis.
30. G. Bayramo˘glu et al. / Journal of Hazardous Materials B101 (2003) 285–300
31. M.Y. Arıca, G. Bayramo˘glu / Journal of Hazardous Materials 149 (2007) 499–507
32. T. Limcharoensuketal./EcotoxicologyandEnvironmentalSafety122(2015)322–330
33. O. Chaalal et al. 2 / Journal of Industrial and Engineering Chemistry xxx (2014) xxx–xxx
34. S. Sun et al. / International Biodeterioration & Biodegradation 108 (2016) 16e23
35. Biosorption of Cd and Ni by inactivated bacteria isolated from agricultural soil treated with
sewage sludge, by Rahim Mohammadzadeh Karakagh.

11. 36. S. Özdemir et al. / Chemical Engineering Journal 152 (2009) 195–206
37. H. Kinoshita et al. / Research in Microbiology xx (2013) 1e9
38. R. Black et al. / Journal of Environmental Chemical Engineering 2 (2014) 1663–1671
effluent.
39. E. Khadivinia et al. / Journal of Industrial and Engineering Chemistry xxx (2014) xxx–xxx.
40. F. Pagnanelli et al. / Bioresource Technology 101 (2010) 2981–2987
41. P. Venkatesh et al. / LWT - Food Science and Technology 68 (2016) 606e614.
42. M. Akbari et al. / Journal of Environmental Chemical Engineering xxx (2014) xxx–xxx
43. T. Wang et al. / Chemosphere 146 (2016) 233e237