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RESEARCH ARTICLE
Calcium alginate entrapped Eupatorium
adenophorum Sprengel stems powder for
chromium(VI) biosorption in aqueous
mediums
Mahendra AryalID*
Department of Chemistry, Tri-Chandra Multiple Campus, Tribhuvan University, Kathmandu, Nepal
*mahendraaryalnp@yahoo.com
Abstract
A novel biosorbent, Eupatorium adenophorum Sprengel-alginate beads was used for chro-
mium(VI) biosorption from aqueous solutions. Biosorption process was optimized at pH 2.0,
biomass concentration 1.0 g/L, contact time 60 min, and temperature 30
o
C respectively.
Maximum uptake capacity of Cr(VI) was calculated at 28.011 mg/g. It was found that the
overall biosorption process was best described by pseudo second-order kinetics with high
correlation coefficient values. Intraparticle diffusion model suggested that Cr(VI) biosorption
may proceed within multiple steps. Data obtained from the batch studies confirmed well to
the Langmuir, Temkin, and Hill-der Boer isotherm models. Scatchard plot analysis further
supported the mono-layer biosorption of Cr(VI) ions on Eupatorium adenophorum Sprengel-
alginate beads as described by Langmuir isotherm model. Numerical values of Eobtained
from Dubinin-Radushkevich isotherm model identified the physisorption as predominant
mechanism for Cr(VI) biosorption. The negative values of ΔG
o
confirmed the spontaneous
and feasibility nature, whereas positive value of ΔH
o
showed the endothermic nature of bio-
sorption process. Positive value of ΔS
o
indicated an increase in the randomness at the
solid/solution interface during the biosorption process. The endothermic nature of Cr(VI) bio-
sorption was also described by Temkin isotherm model. The results indicated that Cr(VI)
biosorption was not significantly affected by the presence of co-ions at lower concentrations.
Desorption of Cr(VI) ions from metal-loaded Eupatorium adenophorum-alginate beads was
observed at 92.091% with 0.5 M HNO
3
solution in solid to liquid ratio of 1.0 g/L.
Introduction
Chromium is a potentially toxic metal originating from anthropogenic activities such as the
mining of chromium ores, iron-steel, electroplating, tanning, printing, dyeing, papermaking,
and textile industries, municipal waste landfill, and sewage irrigation, pesticide, herbicides,
antibiotics, and fertilizer application [1,2,3,4]. Such numerous industries have resulted in a
generation of large quantities of liquid effluent loaded with high concentration of chromium.
PLOS ONE | https://doi.org/10.1371/journal.pone.0213477 August 16, 2019 1 / 21
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OPEN ACCESS
Citation: Aryal M (2019) Calcium alginate
entrapped Eupatorium adenophorum Sprengel
stems powder for chromium(VI) biosorption in
aqueous mediums. PLoS ONE 14(8): e0213477.
https://doi.org/10.1371/journal.pone.0213477
Editor: Moonis Ali Khan, King Saud University,
SAUDI ARABIA
Received: March 15, 2019
Accepted: July 4, 2019
Published: August 16, 2019
Copyright: ©2019 Mahendra Aryal. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: All relevant data are
within the manuscript.
Funding: The author received no specific funding
for this work.
Competing interests: The author has declared that
no competing interests exist.
It is generally found as trivalent and hexavalent states in aqueous environments [1,5]. More
specifically, Cr(III) is relatively non-toxic and required in micro quantities in human food [6].
Under certain conditions, Cr(III) can be oxidized to more carcinogen and mutagen Cr(VI) in
the environment [4,5]. On contrary, Cr(VI) can persist in the long-term in soil and wastewater
because of its non-biodegradability nature [4]. It is known that Cr(VI) is 100 times more toxic
than Cr(III) [1]. Cr(VI) is the most stable species in drinking water, and it can have lethal
effects on human physiological, neurological and biological systems [1,2,3]. Therefore, the
maximum permissible limit of Cr(VI) ions in drinking water has been proposed at 0.1 mg/L
[7].
The quantity of Cr(VI) that exists in industrial effluents released into the environment is
often higher than the acceptable level. Hence, attention should be made to reduce its quantities
from effluents by suitable treatment technologies before it is discharged into the natural envi-
ronment [8]. Different treatment technologies such as precipitation, coagulation, ion
exchange, adsorption, oxidation, reduction, and reverse osmosis techniques have been applied
in order to remove the chromium species from contaminant streams [2]. Each of the methods
exhibits shortcomings such as high operational cost, low removal efficiency, difficult operation
process, limited tolerance to pH change, secondary pollution, and ineffective for small scale
industries [4,9,10]. Due to this reason, there is an immediate action for suitable and cost effec-
tive removal technology for heavy metals [4]. Recently, biosorption has become one of the
alternative methods that has been widely applied for detoxification of heavy metals [1,2]. It has
many advantages over conventional methods such as low cost, easy operating system, high
removal efficiency, removal of metal ions at low concentrations, high metal binding ability,
low biological sludge formation, eco-friendly, recycling of biosorbents, and high recovery of
metal ions from metal-loaded biosorbents [2,6,8].
The bio-materials such as algae, fungi, yeast, bacteria, agricultural and industrial by-prod-
ucts have been studied for removal of heavy metals [1,8,11]. It is reported that biomaterials
have a high potential for heavy metal removal [9,12]. Low cost biosorbents are becoming the
focus of many researches [4]. The plant biosorbents including Acacia albida and Euclea schim-
peri [13], Cicer arientinum [14], Cupressus lusitanica bark [10], eucalyptus bark [15],
helianthus annuus stem waste [16], neem sawdust and mango sawdust [17], mango peels [2],
Plataneusorientalis leaves [18], Polyporus squamosus [19], Senna siamea [6], Stipa tenacissima
[3], Ulmus leaves [20], and wheat bran [21] etc. have been investigated for removal of Cr(VI)
ions from aqueous medium.
Application of native or free biosorbents for removal of heavy metals has some limitations
including low density and mechanical strength, a wide particle size distribution, and poor iso-
lation of solid and liquid phases [22,23,24]. The several matrices have been employed in immo-
bilization of the biosorbents for heavy metal removal in order to overcome such limitations
[25]. The immobilization of biomaterials is very important step for large scale-up of effluents
treatment, and its main advantages include an increase in the density and mechanical strength
of the biomass, easy isolation of solid and liquid phases, retention of biomass within the reac-
tor [23,25]. Use of immobilized biomaterials in industrial scale can reduce separation costs by
60% [23]. Entrapment of biosorbents in the alginate has been used in heavy metal removal,
due to its ease of preparation, biodegradability, hydrophilicity and softness in nature with high
mechanical strength. Alginate is a component of the outer cell wall of brown algae and certain
bacteria. Due to the availability of carboxyl groups, immobilization with alginate can enhance
the efficiency of biosorption of heavy metals [24].
To the best of our knowledge, Eupatorium adenophorum Spreng. stems biomass entrapped
in calcium alginate has not yet been used for Cr(VI) biosorption, thus, it was finally selected to
study in Cr(VI) biosorption. Kinetics, isotherm and desorption studies as well as effect of
Biosorption of Cr(VI) by Eupatorium adenophorum Sprengel biomass
PLOS ONE | https://doi.org/10.1371/journal.pone.0213477 August 16, 2019 2 / 21
interfering ions on Cr(VI) biosorption were studied. The main aim of this research work was
to improve the sequestration potential of immobilized Eupatorium adenophorum biomass for
removing Cr(VI) ions from aqueous solutions.
Materials and methods
Ethics statement
Eupatorium adenophorum Spreng. (Syn. Ageratina adenophorum) is not endangered species
and no specific permission is required for harvesting from the non-protected area in the pur-
pose of scientific research activities. No material was taken from protected area or national
park. Author used stems of this plant that came from his own garden.
Collection of biosorbent
This plant is a widely growing and spreading perennial herbaceous shrub that may grow to 1
or 2 m high, and can cause to damage the grazing land and natural forest (Fig 1). It is locally
known as banmara (killer of the forests) [26]. It was collected from Besisahar Municipality-9,
Nepal. The study site is located at Pakhathok (Latitude 28
o
13’ 42’’ N and Longitude 84
o
22’
22’’ E) with an altitudinal range of 1003 m. Annual average temperature and precipitation/
rainfall are 13.6–25.3˚C and 20–762 mm respectively. Eupatorium adenophorum Spreng. was
indentified according to the criteria as described by Wolff, [27].
Preparation of biosorbent
Eupatorium adenophorum Spreng. stems were first cut into small pieces and dried in sunlight
until all the moisture was evaporated, and then converted into powdered form. After being
powdered, it was treated with 1.0 M HCl in order to remove the impurities as well as to expose
Fig 1. Eupatorium adenophorum Sprengel (Banmara) plant.
https://doi.org/10.1371/journal.pone.0213477.g001
Biosorption of Cr(VI) by Eupatorium adenophorum Sprengel biomass
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more binding sites. It was then washed with distilled water as long as the pH of the washing
solution becomes in neutral range. After washing, moisture content of biomass was deter-
mined by drying a pre-weighted amount in hot air oven (Accumax India) at 100
o
C for 24 h.
Immobilization of biosorbent
Calcium alginate was used as an immobilizing agent for Eupatorium adenophorum Spreng.
stems powder. In this method, two percentage of sodium alginate was first dissolved in distilled
water, and it was mixed with calculated amount of dried Eupatorium adenophorum stems
powder. Eupatorium adenophorum-alginate mixture was then dropped by a syringe into the
5% CaCl
2
solution placed on magnetic stirrer held around 5–8˚C. The beads were hardened in
this solution for 24 h in refrigerator at 4
o
C [11]. The beads were washed with distilled water
for several times to remove excess of calcium ions and un-trapped particles of Eupatorium ade-
nophorum Spreng. biomass. Thus, obtained beads were then air dried. It was found that 1.0 g
of alginated beads contains 0.052 g of dry biomass. The immobilized biomass was used for fur-
ther biosorption experiments.
Preparation of stock metal solution
Stock metal solution was prepared by dissolving the calculated amounts of K
2
Cr
2
O
7
(Merck,
Germany) in distilled water to obtain the standard solutions of 1000 mg/L of Cr(VI) ions. The
desired metal solutions were prepared by dilution of the stock standard solution.
Biosorption experiments
Biosorption experiments were carried out in 50 ml conical flasks. Initial Cr(VI) concentration
of 10 mg/L was used in order to determine the optimum pH, contact time, biomass concentra-
tion and temperature. The Cr(VI) biosorption on Eupatorium adenophorum-alginate beads
was performed with varying initial pH values from 1.0 to 7.0, biomass concentration from 1.0
to 7.0, contact time from 0 to 130 min, and temperature from 20 to 40˚C respectively. Equilib-
rium isotherm experiments were carried out with initial Cr(VI) concentration between 10 and
300 mg/L at pH 2.0, biomass concentration 1.0 g/L and contact time 60 min respectively. All
experiments were performed in triplicate and the mean values were used in the data analysis.
The Cr(VI) concentration was determined at 540 nm followed by complex formation with
1,5-diphenylcarbazide (Merck, Germany) using a spectrophotometer (Shimadzu, Japan) [28].
Effect of interfering ions on Cr(VI) biosorption
Standard solutions of SO
4-2
, Cl
-
, CO
3-2
, Mg
+2
, Ca
+2
, Fe
+3
, Zn
+2
, Cd
+2
, Cu
+2
and Ni
+2
were pre-
pared from Na
2
SO
4
, NaCl, Na
2
CO
3
, MgSO
4
.7H
2
O, CaCl
2
.2H
2
O, FeCl
3
.7H
2
O, ZnSO
4
.7H2O,
CdSO
4
.H
2
O, CuSO
4
.5H
2
O and NiSO
4
.6H
2
O respectively. The effect of interfering ions rang-
ing from 5 to 50 mg/L on Cr(VI) biosorption at 10 mg/L of Cr(VI) ions was conducted.
Desorption studies
Biosorption experiments were first conducted with initial Cr(VI) concentrations of 250 mg/L
at optimum conditions of pH, biomass concentration, contact time and temperature respec-
tively. After Cr(VI) biosorption, Eupatorium adenophorum-alginate beads were collected care-
fully and washed with distilled water. The Cr(VI) ions-adsorbed beads were dried in oven at
60
o
C for 24 h and then again suspended in 30 ml of 0.5 M HNO
3
solution at room tempera-
ture for 2 h.
Biosorption of Cr(VI) by Eupatorium adenophorum Sprengel biomass
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Data analyses
A number of mathematical models have been employed to analyze the experimental data in
order to establish the extent of biosorption of heavy metals. The amount of Cr(VI) ions
adsorbed by Eupatorium adenophorum-alginate beads is given by the following equation;
Qe¼V:ðCoCeÞ
Wð1Þ
Where Q
e
is the amount of Cr(VI) adsorbed by the biomass (mg/g) at equilibrium, C
o
is the
initial concentration of Cr(VI) (mg/L), C
e
is the concentration of Cr(VI) at equilibrium (mg/
L), Vis the initial volume of Cr(VI) solution (L), and Wis the mass of the biosorbent (g).
Langmuir-Hinshelwood (L-H) kinetic model
Langmuir-Hinshelwood (L-H) kinetic model has been applied to determine the adsorption
kinetics of metal ions on biomass surface [29].
lnðCo
CMÞ
ðCoCMÞþko¼k1:t
ðCoCMÞð2Þ
Where k
o
is similar to a zero-order rate constant that represents the initial sorption rate (L/
mol), k
1
is first-order rate constant after sorption reaches its maximum (min
-1
) and C
M
is
metal ion concentration in solution (mol/L). The values of k
1
and k
o
can be determined from
the slope and intercept of a plot between ln(C
o
/C
M
)/(C
o
-C
M
) and t/(Co-C
M
) respectively.
Avrami kinetic model
This kinetic model describes the fractionary kinetic orders. Some parameters of this model
indicate the possible changes in the sorption rates as function of the initial metal ion concen-
tration and adsorption time [30].
lnf lnð1aÞg ¼ nlnkav þnlntð3Þ
Where αis an adsorption fraction (Q
t
/Q
e
) at time t,k
av
is the kinetic constant (min
-1
) and n
is a fractionary kinetic order. The values of nand k
av
can be determined from slope and inter-
cept of a plot of ln{−ln(1 - α)} and lntrespectively.
Lagergren pseudo-first order kinetic model
According to this kinetic model, the rate of occupation of binding sites is proportional to the
number of unoccupied sites [31].
lnðQeQtÞ ¼ lnQek1:tð4Þ
Where k
1
is the pseudo first order rate constant (min
-1
). The values of Q
e
and k
1
can be
obtained from the slope and intercept of a plot between ln(Q
e
−Q
t
) and tat different
temperatures.
Ho pseudo-second order kinetic model
It considers that the rate of occupation of binding sites is proportional to the square of the
number of unoccupied sites [32].
t
Qt¼1
k2Qe2þ ð 1
QeÞ:tð5Þ
Biosorption of Cr(VI) by Eupatorium adenophorum Sprengel biomass
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Eq (5) can be further written as:
t
Qt¼1
hþt
Qeð6Þ
If pseudo-second order kinetic is applicable, the plot of t/Qt versus tgives a straight line
and its slope and intercept give the values of k
2
or h, and Q
e
respectively.
Ritchie pseudo second-order kinetic model
This kinetic model describes that one adsorbate is adsorbed on two binding sites and the rate
of adsorption depends solely on the fraction of the binding sites of adsorbents [33].
1
Qt¼1
krQetþ1
Qeð7Þ
Where k
r
is rate constant of the Ritchie-second order kinetic model (1/min). The value of k
r
can be determined from the slope of a plot between 1/Q
t
and 1/trespectively.
Sobkowsk and Czerwinski pseudo-second order kinetic model
This kinetic model purposes that first order reaction can be applied for lower surface concen-
trations of solid and the second order reaction for higher surface concentrations [34].
y
1y¼k2tð8Þ
Where θ(Q
t
/Q
e
) is the fraction of surface sites, which are occupied by adsorbed metal ions.
The second order rate constant, k
2
(min
-1
) can be calculated from a straight line obtained from
the plot of θ/(1-θ) against trespectively.
Blanachard pseudo-second order kinetic model
Blanachard second order kinetic model initially proposed similar to that of Ritchie’s model for
the exchange reaction of divalent metallic ions onto NH
4+
ions in fixed zeolite particles [35].
1
QeQta¼k2tð9Þ
The rate constant, k
2
(g/mg.min) can be evaluated from the slope of a plot between 1/(Q
e
-
Q
t
) versus trespectively.
Elovich kinetic model
Elovich model can be used to evaluate the kinetics of chemisorption of adsorbate onto hetero-
geneous adsorbent surface [36].
Qt¼1
blnðabÞ þ 1
blntð10Þ
Where αis the initial adsorption rate (mg/gmin), and βis the extent of surface coverage
and activation energy (g/min). If the biosorption data correlate with Elovich equation, a plot of
lntverses Q
t
gives a straight line and the values of βand αcan be determined from its slope
and intercept respectively.
Biosorption of Cr(VI) by Eupatorium adenophorum Sprengel biomass
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Intraparticle diffusion kinetic model
It explains the diffusion mechanism of the biosorption process [37].
Qt¼kid:t0:5þCð11Þ
The value of intraparticle diffusion rate constant (k
id
) can be obtained from the slope of a
linear plot of Q
t
versus t
0.5
, whereas Cis the intercept.
Langmuir isotherm model
According to the Langmuir isotherm model, there are a finite number of binding sites, which
is mono-layer coverage due to homogeneously distributed over the adsorbent surface and
there is no interaction between adsorbed metal ions [38].
Ce
Qe¼Ce
Qmax þ1
Qmax:bð12Þ
Where Q
max
is the maximum uptake capacity (mg/g) and bis the binding affinity (L/mg).
The adsorption feasibility can be evaluated by the Langmuir isotherm separation factor, K
L
.
KL¼1
ð1þb:ceÞð13Þ
The values of K
L
in the range 0 to1 indicate the favorable uptake of metal ions [39].
Scatchard plot analysis
The best fit of Scatchard analysis with experimental equilibrium data suggests that the single
or distinct types of binding sites, which is an indication of mono-layer coverage [40].
Qe
Ce¼Qmax:bQe:bð14Þ
The values Q
max
and bcan be determined from the slope and intercept of a plot between
Q
e
/C
e
and Q
e
respectively.
Freundlich isotherm model
Freundlich isotherm model explains about the multi-layer adsorption of metal ions on hetero-
geneous adsorbent surface [41].
lnQe¼lnKfþ ð1
nÞlnCeð15Þ
Where K
f
and nare the biosorption capacity and intensity respectively. High values K
f
and
1/nsuggest that there is a strong affinity between metal ions and surface binding sites.
Gin isotherm model
Gin et al., [42] proposed a simple equilibrium isotherm model, which can be described by fol-
lowing linear equation;
ln Ce
Co¼1
CoðbMÞ þ lnað16Þ
The value of βand αcan be calculated from the slope and intercept of a plot between ln (C
e
/
C
o
) and 1/C
o
respectively.
Biosorption of Cr(VI) by Eupatorium adenophorum Sprengel biomass
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Temkin isotherm model
This model describes the behavior of adsorption systems on heterogeneous biomass surfaces.
It tells that the heat of sorption of all molecules in a layer decreases linearly due to the adosor-
bent-sorbate interaction [43].
Qe¼BTlnaTþBTlnCeð17Þ
Where;
BT¼RT
bT
Where Tis the absolute temperature (K), Ris the universal gas constant (kJ/mol), b
T
is the heat of adsorption (kJ/mol), and a
T
is equilibrium binding constant (L/mol)
respectively.
Dubinin-Radushkeich (D-R) isotherm model
It indicates the heterogeneity of the surface energies [44].
lnQe¼lnQmb:ε2ð18Þ
Where;
ε¼RTlnð1þ1
CeÞ
Where Q
e
is the amount of metal ions adsorbed by biosorbent (mol/g), C
e
is the concentra-
tion of metal ions in equilibrium (mol/L), βis the adsorption energy (kJ
2
/mol
2
) and Q
m
is the
maximum adsorption capacity (mol/g). The value of βand Q
m
can be evaluated from slope
and intercept of a plot of lnQ
e
against ε
2
. The mean sorption energy (kJ/mol) can be written
as:
E¼1
ffiffiffiffiffiffiffiffiffi
2b
pð19Þ
If the magnitude of Eis in the range of 8 and 16 kJ/mol, the biosorption process is
supposed to be chemisorption, if it is E8 kJ/mol then physisorption is the predominant
mechanism.
Flory-Huggins isotherm model
This isotherm explains the degree of surface coverage characteristics of adsorbate onto adsor-
bent as well as the feasibility and spontaneous nature of an adsorption process [45].
logðCoCeÞ
Co¼log KFH nFH logðCe
CoÞ ð20Þ
Where, K
FH
is the model equilibrium constant (L/mg) and n
FH
its exponent. The standard
Gibb’s free energy (ΔG°) can be calculated as;
DGo¼ RTlnðKFH Þ ð21Þ
The value of standard Gibb’s free energy may give the information about the endothermic or
exothermic nature of biosorption process.
Biosorption of Cr(VI) by Eupatorium adenophorum Sprengel biomass
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Hill-der Boer isotherm model
The Hill-der Boer isotherm model expresses the interactions between adsorbate-adsorbate in
the solid phase and adsorbate-adsorbent at the liquid-solid interface [46].
y
1yþlnðy
1yÞ lnCe¼ lnk2þk1yð22Þ
Where θ(1–C
e
/C
o
) is the surface coverage fraction, k
1
(dimensionless) and k
2
(mg/L) are
constants respectively.
Halsey isotherm model
Hasely isotherm model describes the multi-layer sorption of metal ions on heterogeneous bio-
mass surface [47].
ln Qe¼1
nH
ln KH1
nH
ln Ceð23Þ
The values of n
H
and K
H
can be obtained from the slope and intercept of a linear plot
between lnQ
e
and lnC
e
.
Fundamental thermodynamic parameters
Change in free energy of biosorption, which is a fundamental criterion of spontaneity of the
process. The standard Gibbs free energy change (ΔG
o
) can be calculated from the Langmuir
equilibrium constant at different temperatures [48].
DGo¼ RT lnðbÞ ð24Þ
The experimental data can be further analyzed to evaluate the change in standard enthalpy
(ΔH
o
) and entropy (ΔS
o
) of biosorption process as a function of temperature using van’t Hoff
equation.
ln ðbÞ ¼ DHo
RT þDSo
Rð25Þ
The plot of lnband 1/Tgives a linear line, in which -ΔH
o/
/Rand ΔS
o
/Rare equal to its slope
and intercept respectively.
Results and discussion
Evaluation of precision and accuracy of Cr(VI) concentrations
The calibration curve was made in the linear range of Cr(VI) concentrations from 0.3 to 2 mg/
L with absorbance between 0.159 and 1.137 using a spectrophotometer. The linear regression
result of absorbance against Cr(VI) concentration was A = 0.5704C-0.0012 with correlation
coefficient of 0.9988. Quality control (QC) samples against the number of samples taken are
shown by Fig 2.
The precision is expressed by relative standard deviation and variance methods. Relative
standard deviation (RSD) is a statistical measurement that describes the spread of data with
respect to the mean, and the results are expressed in terms of percentage. The accuracy is
determined as recovery percentage. The precision and accuracy results are presented in
Table 1.
Biosorption of Cr(VI) by Eupatorium adenophorum Sprengel biomass
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Effect of pH
The effect of pH on Cr(VI) biosorption onto Eupatorium adenophorum-alginate beads is shown
in Fig 3. Indeed, the maximum removal of Cr(VI) ions was observed at pH 2.0. Under acidic
conditions, the surface of the biomass becomes highly protonated and binds the Cr(VI) in the
form of HCrO
4-
ions [2,7]. Above pH 2.0, the gradual increase in negatively charged biomass
surface groups as well as shifting of monovalent HCrO
4-
to divalent Cr
2
O
7-2
and CrO
4-2
ions in
aqueous solutions resulted the decrease in Cr(VI) biosorption efficiency [1,6,7,49]. The similar
trends were also observed for Cr(VI) biosorption in various plant biosorbents [3,5,6,10,23,50].
Effect of biomass concentration
As shown in Fig 4, the removal efficiency of Cr(VI) ions was increased with increasing the bio-
mass concentrations from 1.0 to 7.0 g/L respectively. This could be ascribed to the availability
of more binding sites of Eupatorium adenophorum biomass for Cr(VI) ions [10,23]. On the
contrary, the uptake capacities of Cr(VI) ions found to be decreased from 3.915 to 0.667 mg/g
with increase in biomass concentrations from 1.0 to 7.0 g/L (Fig is not shown). It may be due
to the fact that Eupatorium adenophorum-alginate beads has a limited number of active bind-
ing sites for Cr(VI) ions, and it could be achieved the saturation above a certain biomass con-
centration [6,51].
Effect of contact time and temperature
The effect of contact time for Cr(VI) biosorption on Eupatorium adenophorum-alginate beads
at different temperatures is shown in Fig 5. The graphs show that the biosorption efficiency of
Fig 2. Quality control and number of samples.
https://doi.org/10.1371/journal.pone.0213477.g002
Table 1. Precision and accuracy data of Cr(VI) analyses.
QC samples (mg/L) Average (mg/L) SD RSD (%) Variance Recovery (%)
10 9.60 0.219 2.219 0.045 96.088
50 48.697 0.709 0.456 0.502 97.395
100 98.637 0.579 0.512 0.255 98.637
200 198.05 0.627 0.350 0.393 99.025
300 297.238 1.369 0.460 1.876 99.076
https://doi.org/10.1371/journal.pone.0213477.t001
Biosorption of Cr(VI) by Eupatorium adenophorum Sprengel biomass
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Cr(VI) ions increases with increase in contact time. A contact time of 60 min was sufficient to
achieve equilibrium. The results revealed that the removal efficiency of Cr(VI) ions was not
significantly changed with further progress of contact time. On the other hand, Cr(VI) bisorp-
tion efficiency was increased with increase in temperature from 20 to 30
o
C. This may be due
to the increase in collision frequency between Cr(VI) ions and the biomass species [10]. It was
also found that the removal efficiency of Cr(VI) ions was slightly decreased above 30˚C, sug-
gesting the destruction of some binding sites [22,23].
Effect of initial Cr(VI) concentrations
Effect of initial Cr(VI) concentrations on equilibrium uptake capacity at different tempera-
tures is shown in Fig 6. It was found that the amount of equilibrium biosorption capacity
increases with increase in initial Cr(VI) concentrations. High uptake capacity of Cr(VI) ions
Fig 3. Effect of pH on biosorption of Cr(VI) by Eupatorium adenophorum–alginate beads at initial Cr(VI)
concentration 10 mg/L and biomass concentration 1.0 g/L respectively.
https://doi.org/10.1371/journal.pone.0213477.g003
Fig 4. Effect of biomass concentration on biosorption of Cr(VI) by Eupatorium adenophorum–alginate beads at
initial Cr(VI) concentration 10 mg/L and pH 2.0 respectively.
https://doi.org/10.1371/journal.pone.0213477.g004
Biosorption of Cr(VI) by Eupatorium adenophorum Sprengel biomass
PLOS ONE | https://doi.org/10.1371/journal.pone.0213477 August 16, 2019 11 / 21
was observed at lower Cr(VI) concentrations. This may be due to the sufficient binding sites
available on biomass surface. At higher concentrations, relatively less available binding sites
may responsible for reduction of uptake capacity of Cr(VI) species by Eupatorium adeno-
phoru-alginate beads [52]. Similar results have been reported by many authors using different
types of plant biosorbents [3,10,39,52].
Determination of kinetic parameters
Biosorption kinetics can play a vital role to select and design the reactor systems [2]. Various
kinetic models have been used to determine the biosorption rate of heavy metals on biomass
surface. The experimental data were determined to be well predicted by models with
Fig 5. Effect of contact time on Cr(VI) biosorption by Eupatorium adenophorum–alginate beads at initial Cr(VI)
concentration 10 mg/L, pH 2.0 and biomass concentration 1.0 g/L at 20 (-■—), 30 (-×-) and 40˚C (-▲-)
respectively.
https://doi.org/10.1371/journal.pone.0213477.g005
Fig 6. Effect of initial concentration of Cr(VI) ions onto Eupatorium adenophorum-alginate beads at initial Cr
(VI) concentration from 10 to 300 mg/L, pH 2.0, contact time 60 min and biomass concentration 1.0 g/L at 20
(-■—), 30 (-×-) and 40˚C (-▲-) respectively.
https://doi.org/10.1371/journal.pone.0213477.g006
Biosorption of Cr(VI) by Eupatorium adenophorum Sprengel biomass
PLOS ONE | https://doi.org/10.1371/journal.pone.0213477 August 16, 2019 12 / 21
correlation coefficient values closer to unity [5]. Kinetic constants and correlation coefficients
of kinetic models are given in Table 2.
The best correlated kinetic data with Langmuir-Hinshelwood (L-H) kinetic model gives
high correlation coefficient values, which indicates the chemisorption as a predominant mech-
anism [29]. The low R
2
values at different temperatures showed that this model can not be
applied to predict the biosorption kinetics. However, Cr(VI) biosorption may be proceeded
with physisorption mechanism [12].
Avrami model describes the possible changes of biosorption mechanism with multiple
kinetic orders [30]. In this study, low R
2
values indicated that kinetic data of Cr(VI) biosorp-
tion on Eupatorium adenophorum-alginate beads were not agreement with Avrami model.
The fitness of Cr(VI) biosorption data with low correlation coefficients as well as lower Q
e,
cal
comparison to Q
e,exp
indicated that Cr(VI) biosorption on Eupatorium adenophorum-algi-
nate beads did not follow Lagergren pseudo-first order reaction [12].
The results showed that the regression (R
2
) values of Ho pseudo second order model were
nearly unity. Results confirmed that biosorption data were well represented by Ho pseudo
Table 2. Kinetic parameters of Cr(VI) sorption on Eupatorium adenophorum–alginate beads at initial Cr(VI) concentration 10 mg/L, pH 2.0 and biomass concen-
tration 1.0 g/L respectively.
Kinetic model Parameter Temperature
20˚C 30˚C 40˚C
Q
e,exp
(mg/g) 3.820 4.669 4.198
Langmuir-Hinshelwood k
1
(min
-1
) 0.008 0.001 0.009
k
0
(L/mg) 0.103 0.108 0.107
k
1
/k
0
(mg/L.min) 0.007 0.010 0.0083
R
2
0.848 0.857 0.835
Avrami n0.861 0.743 0.811
k
av
(min
-1
) 0.082 0.180 0.126
R
2
0.961 0.936 0.933
Lagergren pseudo-first order k
1
(min
-1
) 0.057 0.052 0.0529
Q
e,
(mg/g) 6.382 5.353 5.228
R
2
0.877 0.931 0.921
Ritchie pseudo second-order Q
e
(mg/g) 4.486 3.861 4.163
k
2
(min
-1
) 0.105 0.060 0.088
R
2
0.859 0.950 0.892
Sobkowsk and Czerwinski pseudo
second-order
k
2
(min
-1
) 0.302 0.260 0.397
R
2
0.790 0.900 0.753
Blanachard pseudo second-order k
2
(g/mg min) 0.079 0.0563 0.0946
α(g/mg) 1.758 0.809 1.884
R
2
0.830 0.890 0.901
Ho pseudo second-order k
2
(gm/g min) 0.0079 0.0085 0.0084
h(mg/g)/min 0.161 0.259 0.220
Q
e
(mg/g) 4.710 5.494 5.107
R
2
0.980 0.988 0.987
Elovich α(mg/g.min) 2.700 5.143 3.214
β(g/mg) 1.054 2.313 1.537
R
2
0.952 0.953 0.953
Intraparticle diffusion k
id
(mg/g min
0.5
) 0.327 0.354 0.336
C(mg/g) 0.422 1.041 0.819
R
2
0.938 0.932 0.928
https://doi.org/10.1371/journal.pone.0213477.t002
Biosorption of Cr(VI) by Eupatorium adenophorum Sprengel biomass
PLOS ONE | https://doi.org/10.1371/journal.pone.0213477 August 16, 2019 13 / 21
second order model. Additionally, it was also found that the Q
e,exp
values were good agreement
with the Q
e,cal
ones. The rate constant (k
2
) and initial sorption rate (h) values were higher at 30
o
C comparison to the other studied temperatures, indicating that the biosorption of Cr(VI)
species becomes faster at 30
o
C [32].
The comparatively low correlation coefficient values were observed with Ritchie, Sobkowsk
and Czerwinski, and Blanachard pseudo second-order kinetic models respectively. Results
indicated that biosorption process was not well described with these kinetic models [12].
The best correlation of experimental kinetic data to the Elovich kinetic model is the evi-
dence of chemisorption process. Relatively low R
2
values at all temperature was not suggested
this model for Cr(VI) biosorption onto Eupatorium adenophorum-alginate beads [36].
Intraparticle diffusion model identifies the diffusion mechanisms and rate controlling steps
affecting the biosorption process. The smaller values of R
2
evidenced that experimental kinetic
date were not fitted the model very well. It was also found that values of k
id
increased with
increasing temperature from 20 to 30
o
C and then decrease to 40
o
C. Larger values of k
id
may
suggest the faster diffusion. On the contrary, increase in values of Cindicated the increase in
the thickness of the boundary layer and decrease in chance of the external mass transfer. The
plots of Q
t
versus t
0.5
at different temperatures are given in Fig 7. The multi-linearity of plots
indicated that Cr(VI) biosorption may take place in multiple steps [5,6]. First linear portions
may suggest the boundary layer diffusion of Cr(VI) ions, whereas those of second portions
may suggest the intraparticle diffusion starts to slow down due to the extremely low Cr(VI)
concentration left in the biosorption medium [37].
Biosorption isotherms
The extent of biosorption can be correlated in terms of an adsorption isotherm and it explains
the interaction between the adsorbate and adsorbent in biosorption process. The isotherm
models parameters along with regression coefficients on Cr(VI) biosorption were investigated
and the results are listed in Table 3.
The application of Langmuir isotherm plots for Cr(VI) biosorption at different temperatures is
shown in Fig 8. The maximum uptake capacity of Eupatorium adenophorum-alginate beads for
Fig 7. Intraparticle diffusion plots of Cr(VI) biosorption at initial concentration 10 mg/L, pH 2.0 and biomass
concentration 1.0 g/L at 20 (-■—), 30 (-×-) and 40˚C (-▲-) respectively.
https://doi.org/10.1371/journal.pone.0213477.g007
Biosorption of Cr(VI) by Eupatorium adenophorum Sprengel biomass
PLOS ONE | https://doi.org/10.1371/journal.pone.0213477 August 16, 2019 14 / 21
Cr(VI) was calculated at 28.011 mg/g at optimum conditions. The comparative analysis of R
2
val-
ues indicated that the Cr(VI) biosorption was best described by Langmuir model. It may be attrib-
uted to the homogeneous distribution of binding sites on biomass surface and mono-layer
sorption of Cr(VI) species [6]. It also suggested that there was no interaction between Cr(VI) ions
adsorbed on neighboring binding sites. Moreover, K
L
values were between 0 and 1, which con-
firmed the viability of Cr(VI) biosorption on Eupatorium adenophorum-alginate beads [39]. A
comparison of maximum uptake capacity of Cr(VI) on Eupatorium adenophorum-alginate beads
with different plant biosorbents reported in the literature is presented in Table 4.
Fig 9 shows the Scatchard plots for Cr(VI) biosorption on Eupatorium adenophorum-algi-
nate beads at different temperatures. The higher values of R
2
indicated the satisfactory fitting
of the experimental data. It confirmed that the binding sites of this biosorbent exhibited the
same affinity towards Cr(VI) ions, and further supported the mono-layer biosorption process
as described by Langmuir isotherm model [40].
Freundlich isotherm model gave a less reasonable fit to the experimental data comparison
to Langmuir model, indicating that biosorption of Cr(VI) ions was not followed by this
Table 3. Isotherm parameters of Cr(VI) sorption on Eupatorium adenophorum–alginate beads at initial Cr(VI) concentration from 10 to 300 mg/L, pH 2.0 and bio-
mass concentration 1.0 g/L respectively.
Isotherm model Parameter Temperature
20
o
C 30
o
C 40
o
C
Langmuir Q
max
(mg/g) 20.611 28.011 25.575
b(L/mg) 0.0291 0.0292 0.0272
K
L
0.109–0.837 0.111–0.853 0.117–0.854
R
2
0.997 0.999 0.999
Scattered Q
max
(mg/g) 21.035 27.744 26.007
b(L/mg) -0.027 -0.029 -0.026
R
2
0.964 0.984 0.982
Freundlich K
f
(L/g) 1.609 2.212 1.773
n2.151 2.119 2.055
R
2
0.946 0.938 0.951
Gin α0.899 0.862 0.876
β(mg/L.g) -3.168 -4.014 -3.520
R
2
0.855 0.818 0.843
Temkin b
T
(kJ/mol) 0.574 0.460 0.495
a
T
(L/mol) 0.332 0.382 0.317
R
2
0.993 0.997 0.997
D-R Q
m
(mg/g) 51.879 70.275 66.879
E(kJ/mol) 9.128 10 10
R
2
0.978 0.965 0.978
Hill-der Boer k
1
21.981 19.089 20.559
lnk
2
9.391 9.391 9.468
R
2
0.993 0.994 0.996
Flory-Huggins n
FH
-0.317 -0.283 -0.306
K
FH
(L/mg) 0.992 0.989 0.990
ΔG
o
(kJ/mol) -18.513 -25.695 -26.022
R
2
0.955 0.955 0.942
Halsey n
H
-2.151 -2.133 -2.055
K
H
(L/mg) 0.359 0.198 0.307
R
2
0.946 0.932 0.951
https://doi.org/10.1371/journal.pone.0213477.t003
Biosorption of Cr(VI) by Eupatorium adenophorum Sprengel biomass
PLOS ONE | https://doi.org/10.1371/journal.pone.0213477 August 16, 2019 15 / 21
isotherm model. However, values of Freundlich constant, nin the range of 2 to10 suggested
that Cr(VI) sorption was favorable on Eupatorium adenophorum-alginate beads [41].
The fairly low linear regression (R
2
) values were not ascertained the good fitness of equilib-
rium data for Gin isotherm model. But, the negative values of βconfirmed the feasibility of Cr
(VI) biosorption on Eupatorium adenophorum-alginate beads [42].
The high values of R
2
obtained from equilibrium data showed the applicability of Temkin
isotherm model for Cr(VI) biosorption on Eupatorium adenophorum-alginate beads. The val-
ues of heat of biosorption, b
T
are positive at all temperatures, which may suggest the Cr(VI)
biosorption was endothermic in nature. On the other hand, lower values of b
T
suggested the
weak interaction between Cr(VI) ions and binding sites [43].
In all cases, Dubinin-Radushkevich (D-R) isotherm model exhibited lower correlation coef-
ficient values. Also, the values of maximum uptake capacities determined were much higher
than those of experimental values. Therefore, D-R isotherm model was unable to describe the
Fig 8. Langmuir isotherm for Cr(VI) ions onto Eupatorium adenophorum–alginate beads at initial Cr(VI)
concentration from 10 to 300 mg/L, pH 2.0, contact time 60 min and biomass concentration 1.0 g/L at 20 (-■—),
30 (-×-) and 40˚C (-▲-) respectively.
https://doi.org/10.1371/journal.pone.0213477.g008
Table 4. Comparison of Cr(VI) uptake capacity with other plant biosorbents.
Biosorbent Q
max
(mg/g) Reference
Cupressus lusitanica bark 305.4 [10]
Senna siamea seed 139.86 [6]
Cicer arientinum 72.16 [14]
Mango peels 66.66 [2]
Polyporus squamosus 31.2 [19]
Eupatorium adenophorum-alginate beads 28.011 Present study
Stipa tenacissima L18.51 [3]
Eichhorniacrassipes 6.0 [53]
Plataneusorientalis leaves 5.01 [18]
Euclea schimperi 3.946 [13]
Acacia albida 2.983 [13]
Wheat bran 0.942 [21]
Ulmus leaves 0.9 [20]
https://doi.org/10.1371/journal.pone.0213477.t004
Biosorption of Cr(VI) by Eupatorium adenophorum Sprengel biomass
PLOS ONE | https://doi.org/10.1371/journal.pone.0213477 August 16, 2019 16 / 21
Cr(VI) biosorption onto Eupatorium adenophorum-alginate beads. In addition, the numerical
values of Esuggested the physisorption was predominant mechanism for Cr(VI) biosorption
[6,44].
The degree of surface coverage of the biomass can be studied by Flory-Huggins model. The
correlation coefficient values may imply the moderate applicability of Cr(VI) biosorption.
Negative values of Gibbs free energy indicated the spontaneous nature and feasibility of Cr
(VI) biosorption on Eupatorium adenophorum-alginate beads [12,45].
High correlation coefficient values revealed that Hill-der Boer model is the best prediction
of Cr(VI) biosorption on Eupatorium adenophorum-alginate beads. The strong interaction
between Cr(VI) ions and Eupatorium adenophorum surface binding sites was supported by the
higher values of k
1
and lower values of k
2
respectively [46].
Hasely isotherm model describes the surface heterogeneity of biomass surface and multi-
layer biosorption process. The calculated values of correlation coefficient indicated that multi-
layer sorption was not involved in Cr(VI) biosorption on Eupatorium adenophorum-alginate
beads [47].
Thermodynamic analysis
The fundamental thermodynamic parameters for biosorption of Cr(VI) ions on Eupatorium
adenophorum-alginate beads at different temperature are depicted in Table 5. The negative val-
ues of ΔG
o
obtained at all temperatures confirmed the spontaneous and feasibility nature of Cr
(VI) biosorption process [3,5,6]. Magnitudes of ΔG
o
suggested the Cr(VI) biosorption on
Eupatorium adenophorum–alginate beads imply the physisorption mechanism [54]. Positive
Fig 9. Scatchard plots for Cr(VI) ions onto Eupatorium adenophorum–alginate beads at initial Cr(VI)
concentration from 10 to 300 mg/L, pH 2.0, contact time 60 min and biomass concentration 1.0 g/L at 20 (-■—),
30 (-×-) and 40˚C (-▲-) respectively.
https://doi.org/10.1371/journal.pone.0213477.g009
Table 5. Thermodynamic parameters of Cr(VI) biosorption onto Eupatorium adenophorum-alginate beads.
C
o
(mg/L) T(
o
C) Thermodynamic parameters
ΔG
o
(kJ mol
−1
)ΔH
o
(kJ mol
−1
)ΔS
o
(J mol
−1
K)
10 20–40 -18.156 to-18.323 2.612 53.549
https://doi.org/10.1371/journal.pone.0213477.t005
Biosorption of Cr(VI) by Eupatorium adenophorum Sprengel biomass
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value of ΔH
o
showed the endothermic nature of biosorption process [2,3]. In addition, the cal-
culated values of ΔH
o
further supported to the physisorption as operation phenomenon [55].
Moreover, the positive value of entropy change (ΔS
o
) indicated an increase in the randomness
at the solid/solution interface during the biosorption process [3].
Effect of interfering co-ions
The co-ions present in wastewater may compete with primary metal ions on limited binding
sites, which can reduce the biosorption performance in operating systems [29]. Table 6 shows
the effect of co-existing ions on Cr(VI) biosorption onto Eupatorium adenophorum-alginate
beads. Results demonstrated that Cr(VI) biosorption performance was not significantly
affected by the presence of Mg
+2
, Ca
+2
, Zn
+2
, Cd
+2
, Cu
+2
and Ni
+2
ions in studied concentra-
tions, suggesting that such ions were unable to chelate the surface binding sites [12]. On the
other hand, Cr(VI) biosorption efficiency was found to be slightly decreased with increase in
concentration of SO
4—
, Cl
-
, and CO
3-
ions, indicating the competitive phenomenon of same
charged species in the same binding sites [29]. Furthermore, sorption efficiency of Cr(VI)
increased with increasing the concentration of Fe
+3
ions. This may be attributed to the Fe
+3
ions on biomass surface may generate the new binding sites for Cr(VI) ions on biomass surface
[56].
Desorption studies
The desorption of Cr(VI) ions from metal-loaded Eupatorium adenophorum-alginate beads
was observed at 92.091% using 0.5 M HNO
3
solution at room temperature. High desorption
efficiency of Cr(VI) ions from the biomass surface within a short period may confirm the weak
interaction between Cr(VI) ions and binding sites [56]. Relatively low desorption efficiency
(65%) of Cr(VI) ions from Casurina equisetifolia biomass has also reported by Ranganathan,
[40].
Conclusions
Calcium alginate entrapped Eupatorium adenophorum Spreng.stems powder biomass showed
the high removal efficiency for removal of Cr(VI) species from aqueous solutions. It was found
that biosorption kinetics fitted well with pseudo-second order among different kinetic models
owing to high R
2
values. Due to high values of the correlation coefficient, sorption equilibrium
data followed by Langmuir, Temkin and Hill-der Boer isotherm as compared to other iso-
therm models. Scatchard plots analysis indentified the mono-layer biosorption process as
described by Langmuir isotherm model. Cr(VI) biosorption was not significantly affected by
the presence of interfering co-ions at lower concentrations. Thermodynamic parameters val-
ues demonstrated that the endothermic, spontaneous and feasibility nature of Cr(VI) biosorp-
tion on Eupatorium adenophorum-alginate beads. Temkin and Dubinin-Radushkevich
isotherm models as well as ΔG
o
and ΔH
o
values at all the studied temperatures suggested that
Table 6. Effect of interfering ions on Cr(VI) biosorption at initial concentration of 10 mg/L at optimum conditions.
Co-ions (mg/L) Cr(VI) removal (%)
SO
4-2
Cl
-
CO
3-2
Mg
+2
Ca
+2
Fe
+3
Zn
+2
Cd
+2
Cu
+2
Ni
+2
5 41.10 43.53 43.08 38.18 38.22 43.08 41.08 44.55 41.09 36.01
10 40.03 38.18 40.58 38.03 39.81 46.77 41.75 38.99 38.50 38.55
25 41.61 38.97 41.12 40.89 41.38 51.04 39.65 42.05 40.28 39.11
50 37.78 36.71 36.97 42.66 38.74 59.33 40.47 42.13 42.00 42.67
https://doi.org/10.1371/journal.pone.0213477.t006
Biosorption of Cr(VI) by Eupatorium adenophorum Sprengel biomass
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physisorption was the predominant mechanism for Cr(VI) biosorption. High desorption effi-
ciency of Cr(VI) ions from the Cr(VI)-loaded biomass using dilute HNO
3
solution within a
short period may confirm the weak interaction between Cr(VI) ions and biomass binding sites
It can be concluded from these results that Eupatorium adenophorum-alginate beads can be
used as an efficient and eco-friendly biosorbent for the Cr(VI) removal from aqueous media.
Author Contributions
Data curation: Mahendra Aryal.
Formal analysis: Mahendra Aryal.
Investigation: Mahendra Aryal.
Methodology: Mahendra Aryal.
References
1. Cui Y, He H, Atkinson JD. Iron/Carbon Composites for Cr(VI) removal prepared from harmful algal
bloom biomass via metal bioaccumulation or biosorption. ACS Sustainable Chem Eng 2018; https://doi.
org/10.1021/acssuschemeng.8b04921
2. Haq A, Saeed M, Usman M, Yameen M, Muneer M, Tubbsum S, et al. A comparative sorption study of
Cr
3+
and Cr
6+
using mango peels: kinetic, equilibrium and thermodynamic. Green Process Synth 2019;
8: 337–347.
3. Samir L, Samira A, Mekatel Eh, Djamel N. Adsorption of Cr(VI) on Stipa tenacissima L (Alfa): Character-
istics, kinetics and thermodynamic studies. Separ Sci Technol 2018; https://doi.org/10.1080/01496395.
2018.1521833
4. Xia S, Song Z, Jeyakumar P, Shaheen SM, Rinklebe J, Ok YS, Bolan N, Wang H, et al. A critical review
on bioremediation technologies for Cr(VI)-contaminated soils and wastewater. Crit Rev Environ Sci
Technol 2019; https://doi.org/10.1080/10643389.2018.1564526
5. Danish M, Hashima R, Ibrahim MNM, Rafatullah M, Sulaiman O. Surface characterization and compar-
ative adsorption properties of Cr(VI) on pyrolysed adsorbents of Acacia mangium wood and Phoenix
dactylifera L. stone carbon. J Anal Appl Pyrolysis 2012; 97: 19–28.
6. Ajmani A, Shahnaz T, Narayanan S, Narayanaswamy S. Equilibrium, kinetics and thermodynamics of
hexavalent chromium biosorption on pristine and zinc chloride activated Senna siamea seed pods.
Chem Ecol 2019; https://doi.org/10.1080/02757540.2019.1584614
7. Palmer CD, Puls RW. Natural attenuation of hexavalent chromium in ground water and soils. U.S. EPA
ground water issue paper, EPA/540/5-94/505 (U.S. EPA, Office of Research and Development, Wash-
ington. 1994.
8. Vakili M, Rafatullah M, Ibrahim MH, Abdullah AZ, Salamatinia B, Gholami Z, et al. Oil palm biomass as
an adsorbent for heavy metals. Rev. Environ. Contamin. Toxicol., 2014; 232: 61–88.
9. Ahmad T, Rafatullah M, Ghazali A, Sulaiman O, Hashim R. Oil palm biomass-based adsorbents for the
removal of water pollutants-A review. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev. 2011;
29: 177–222. https://doi.org/10.1080/10590501.2011.601847 PMID: 21929380
10. Netzahuatl-Muñoz AR, Cristiani-Urbina MC, Cristiani-Urbina E. Chromium biosorption from Cr(VI)
aqueous solutions by Cupressus lusitanica bark: Kinetics, equilibrium and thermodynamic studies.
PLoS ONE. 2015; 10(9): e0137086. https://doi.org/10.1371/journal.pone.0137086 PMID: 26352933
11. Ozdemir G, Ceyhan N, Manav E. Utilization in alginate beads for Cu (II) and Ni (II) adsorption of an exo-
polysaccharide produced by Chryseomonas luteola TEM05. World J Microbiol Biotechnol. 2005; 21:
163–167.
12. Aryal M, Liakopoulou-Kyriakides M. Characterization of Mycobacterium sp. Strain Spyr1 biomass and
its biosorption behavior towards Cr(III) and Cr(VI) in single, binary and multi-ion aqueous systems. J
Chem Technol Biotechnol. 2013; 89: 559–568.
13. Gebrehawaria G, Hussen A, Rao VM. Removal of hexavalent chromium from aqueous solutions using
barks of Acacia albida and leaves of Euclea schimperi. Inter J Environ Sci Technol. 2015; 12: 1569–
1580
14. Ahalya N, Kanamadi R.D, Ramchandra TV. Biosorption of iron(III) from aquoues solutions using the
husk of Cicer arientinum. Indian J Chem Technol. 2006; 13: 122–127.
Biosorption of Cr(VI) by Eupatorium adenophorum Sprengel biomass
PLOS ONE | https://doi.org/10.1371/journal.pone.0213477 August 16, 2019 19 / 21
15. Sarin V, Pant KK. Removal of chromium from industrial waste by using eucalyptus bark. Bioresour
Technol. 2006; 97:15–20
16. Jain M, Garg VK, Kadirvelu K. Chromium(VI) removal from aqueous system using Helianthus Annus
(sunflower) stem waste. J Hazard Mater. 2009; 162: 365–372.
17. Vinodhini V, Das N. Biowaste materials as sorbents to remove chromium (VI) from aqueous environ-
ment- a comparative study. ARPN J Agr Biol Sci. 2009; 6:19–23.
18. Mahvi AH, Nabizadeh R, Gholami F, Khairi A. Adsorption of chromium from wastewater by Platanus
oriantalis leaves. Iranian J Environ Heal Sci Eng. 2007; 4: 191–196.
19. Razmovski R, Sciban M. Iron(III) biosorption by Polyporus squamosu. African J Biotechnol. 2008; 7:
1693–1699.
20. Gholami-burujeni F, Mahvi A, Omrani GhA., Nazmara S, Gashri A. Removal of Chromium (VI) from
aqueous solution by Ulmus leaves. Iranian J Environ Heal Sci Eng. 2006; 3: 97–102.
21. Nameni M, Moghadam MRA, Arami M. Adsorption of hexavalent chromium from aqueous solutions by
wheat bran. Int J Environ Sci Technol. 2008; 5:161–168.
22. Aryal M, Liakopoulou-Kyriakides M. Bioremoval of heavy metals by bacterial biomass. Environ Monit
Assess 2015, 187: 4173. https://doi.org/10.1007/s10661-014-4173-z PMID: 25471624
23. Khorramabadi GS, Soltani RDC, Rezaee A, Khataee AR, Jafari AJ. Utilisation of immobilised activated
sludge for the biosorption of chromium (VI), Can J Chem Eng. 2011; 9999:1–8.
24. Onal SS, Baysal H, Ozdemir G. Studies on the applicability of alginate-Entrapped Chryseomonas
luteola TEM 05 for heavy metal biosorption. J Hazard Mater. 2007; 146: 417–420.
25. Luan TG, Jin J, Chan SMN, Wong YS, Tam NFY. Biosorption and biodegradation of Tributyltin (TBT) by
alginate immobilised Chlorella vulgaris beads in several treatment cycles. Process Biochem. 2006; 4:
1560–1565.
26. Shrestha K, Wilson E, Gay H. Ecological and environmental study of Eupatorium adenophorum Spren-
gel (Banmara) with reference to its gall formation in Gorkha-Langtang route. Nepal J Nat Hist Mus.
2008; 23: 108–124.
27. Wolff MA. (1999). Winning the war of weeds: The essential gardener’s guide to weed identification and
control. Kenthurst, NSW, Kangaroo Press. 1999; p:17, ISBN 0-86417-993-6.
28. Snell FD, Snell CT. Colorimetric methods of analysis. 3
rd
ed. Van Nostrand, New York. 1959.
29. Texier A-C, Andres Y, Cloirec P. Selective Biosorption of Lanthanide (La, Eu, Yb) Ions by Pseudomo-
nas aeruginosa. Environ Sci Technol. 1999; 33: 489–495.
30. Njoku VO, Ayuk AA, Oguzie EE, Ejike EN. Biosorption of Cd(II) from aqueous solution by Cocoa Pod
husk biomass: Equilibrium, kinetic, and thermodynamic studies. Separ Sci Technol. 2012; 47: 753–
761.
31. Lagergren S. Zur theorie der sogenannten adsorption gelo
¨ster stoffe, Kungliga Svenska Vetenskapsa-
kad. Handlingar. 1898; 24: 1–39.
32. Ho YS, McKay G. Pseudo-second order model for sorption processes. Process Biochem. 1999; 34:
451–465.
33. Zhou Y-T, Branford-White C, Nie H-L, Zhu L-M. Adsorption mechanism of Cu
2+
from aqueous solution
by chitosan-coated magnetic nanoparticles modified with α-ketoglutaric acid. Colloids Surf B Biointer-
faces 2009; 74: 244–252.
34. Sobkowsk J, Czerwinski A. Kinetics of carbon dioxide on a platinum electrode. J Electroanal Chem.
1974; 55: 391–7.
35. Blanachard G, Maunaye M, Martin G. Removal of heavy metals from waters by means of natural zeo-
lites. Water Res. 1984; 18: 1501–1507.
36. Rudzinski W, Panczyk T. Kinetics of isothermal adsorption on energetically heterogeneous solid sur-
faces: A new theoretical description based on the statistical rate theory of interfacial transport. J Physi-
cal Chem B. 2000; 104: 9149–9162.
37. Weber Jr WJ, Morris JC. Kinetics of adsorption on carbon from solution. J Sanit Eng-ASCE 1963; 89:
31–59.
38. Langmuir I. The adsorption of gases on plane surfaces of glass, mica, and platinum. J Am Chem Soc.
1918; 40: 1361–1367.
39. Hadi M, Samarghandi MR, McKay G. Equilibrium two-parameter isotherms of acid dyes sorption by acti-
vated carbons: Study of residual errors. Chem Eng J 2010; 160: 408–416.
40. Scatchard G. The attractions of proteins for small molecules and ions. Ann N Y Acad Sci. 1949; 51:
660–672.
Biosorption of Cr(VI) by Eupatorium adenophorum Sprengel biomass
PLOS ONE | https://doi.org/10.1371/journal.pone.0213477 August 16, 2019 20 / 21
41. Freundlich H. Ueber die adsorption in Loesungen. Zeitschrift fu¨r Physikalische Chemie 1906; 57: 385–
470.
42. Gin KY-H, Tang Y-Z, Aziz MA. Derivation and application of a new model for heavy metal biosorption by
algae. Water Res. 2002; 36: 1313–1323.
43. Temkin MJ, Pyzher V. Recent modifications to Langmuir isotherms. Acta Phsysio-chem sinica 1940;
12: 217–222.
44. Dubinin MM, Zaverina ED, Radushkevich LV. Sorption and structure of active carbons. I. Adsorption of
organic vapors. Zhurnal Fizicheskoi Khimii. 1947; 21: 1351–1362.
45. Horsfall M Jr, Spiff I. Equilibrium sorption study of Al
3+
, Co
2+
and Ag
+
in aqueous solutions by fluted
pumpkin (Telfairia occidentalis HOOK f) waste biomass. Acta Chim Slov. 2005, 52, 174–181.
46. Wang XS, Li ZZ, Sun C. A comparative study of removal of Cu(II) from aqueous solutions by locally low-
cost materials: marine macroalgae and agricultural by-products. Desalination. 2009; 235: 146–159.
47. Halsey G. Physical adsorption on non-uniform surfaces. J Chem Phys. 1948; 16: 931–937.
48. Aryal M, Ziagova M, Liakopoulou-Kyriakides M. Comparison of Cr(VI) and As(V) removal in single and
binary mixtures with Fe(III)-treated Staphylococus xylosus biomass: Thermodynamic studies. Chem
Eng J 2011; 169: 100–106.
49. Levankumar L, Muthukumaran V, Gobinath MB. Batch adsorption and kinetics of chromium (VI)
removal from aqueous solutions by Ocimum americanum L. seed pods. J Hazard Mater. 2009; 161:
709–713.
50. Namasivayam C, Sangeetha D, Gunasekaran R. Removal of anions, heavy metals, organics and dyes
from water by adsorption onto a new activated carbon from Jatropha husk, an groindustrial solid waste.
Process Saf Environ Protect. 2007; 85: 181–184.
51. Ranganathan K. Chromium removal by activated carbons prepared from Casurina Equisetifolia leaves.
Bioresour Technol. 2000; 73: 99–103.
52. Acharya J, Sahu JN, Sahoo BK, Mohanty CR, Meikap BC. Removal of chromium(VI) from wastewater
by activated carbon developed from Tamarind wood activated with zinc chloride. Chem Eng J. 2009;
150: 25–39.
53. Lytle CM, Lytle FM, Yang N, Qian JH, Hansen D, Zayed A, Teroy N, et al. Reduction of Cr (VI) to Cr (III)
by plants: Potential for in situ heavy metal detoxification. Environ Sci Technol. 1998; 32: 3087–3093.
54. Horsfall M Jr, Abia AA, Spiff AI. Kinetic studies on the adsorption of Cd2+, Cu2+ and Zn2+ ions from
aqueous solutions by cassava (Manihot sculenta Cranz) tuber bark waste. Bioresour Technol. 2006;
97: 283–291.
55. Sag Y, Kutsal T. Determination of the biosorption heats of heavy metal ions on Zoogloea ramigera and
Rhizopus arrhizus. Biochem Eng J. 2000; 6: 145–151.
56. Aryal M, Ziagova M, Liakopoulou-Kyriakides M. Study on arsenic biosorption using Fe(III)-treated bio-
mass of Staphylococcus xylosus. Chem Eng J. 2010; 162: 178–185.
Biosorption of Cr(VI) by Eupatorium adenophorum Sprengel biomass
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