Biosorption of methylene blue onto Arthrospira platensis biomass:Kinetic, equilibrium and thermodynamic studies

Dimitris Mitrogiannis a,*, Giorgos Markou a, Abuzer Çelekli b, Hüseyin Bozkurt c

aDepartment of Natural Resources Management and Agricultural Engineering, Agricultural University of Athens, Iera Odos 75, Athens 11855, GreecebDepartment of Biology, Faculty of Art and Science, University of Gaziantep, Gaziantep 27310, TurkeycDepartment of Food Engineering, Faculty of Engineering, University of Gaziantep, Gaziantep 27310, Turkey

A R T I C L E I N F O

Article history:Received 12 November 2014Accepted 11 February 2015Available online 17 February 2015

Keywords:Arthrospira platensisMethylene blueCationic dyeThermodynamicsBiosorption mechanismCation exchange

A B S T R A C T

In this study, Arthrospira platensis biomass was employed as a biosorbent for the removal of methyleneblue (MB) dye from aqueous solutions. The kinetic data were better described by the pseudo-secondorder model and equilibrium was established within 60–120 min. The intra-particle diffusion was not theonly rate-limiting step and film diffusion might contribute to MB biosorption process. The increase oftemperature from 298 to 318 K caused a decrease of biosorption capacity. The Langmuir, Freundlich andDubinin–Radushkevich (D–R) isotherm models described well the experimental equilibrium data at allstudied temperatures. The maximum monolayer adsorption capacity (qmax) was 312.5 mg MB/g at 298 Kand pH 7.5. According to the results of the thermodynamic analysis and the release of exchangeablecations from the biomass surface, physical sorption and ion exchange were the dominant mechanisms ofMB biosorption at lower temperature. Methanol esterification of the dried biomass showed theinvolvement of carboxyl functional groups in MB chemisorption. The thermodynamic parametersindicated that MB biosorption onto A. platensis was a spontaneous, favorable and exothermic process. Thebiosorption results showed that A. platensis could be employed as an efficient and eco-friendly biosorbentfor the removal of cationic dyes.

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Introduction

Synthetic dyes are hazardous pollutants which present toxicand aesthetic effects in aquatic environments. Dye effluents,containing colored organic molecules, increase the organic load ofwater bodies and reduce the sunlight penetration, affecting thephotosynthetic activity of phytoplankton and disturbing theecological balance of the aquatic environments. Moreover, somedyes display carcinogenic and mutagenic activity [1,2]. Potentialsources of dyes are textile, leather, paper, printing, plastic,electroplating, food and cosmetic industries.

Various physical, chemical and biological methods have beeninvestigated for the treatment of wastewaters contaminated withsynthetic dyes [3]. However, each of these technologies has itsdisadvantages, such as high operational and initial capital costs, lowefficiency at low dye concentrations and production of undesirablesludge [4]. Among treatment technologies, adsorption is consideredas an effective method for dye removal using low-cost materials.

Although activated carbon is the most commonly used adsorbentand is veryefficient to remove dyes fromwastewater, it presents highcosts of production and regeneration [5]. A number of studies havebeen made to find cost-effective and eco-friendly methods fortreatment of dye wastewaters using cheep biomaterials as adsorb-ents [3].

Algae and cyanobacteria have gained interest as alternativebiosorbents due to their high binding affinity, their higher sorptionselectivity for pollutants than commercial ion-exchange resins andactivated carbon, and due to their capability of growing usingwastewater as cultivation medium [3,4,6,7]. The filamentouscyanobacterium Arthrospira platensis is a potential biosorbent,having several advantages, such as relative high growth rates, highbiomass productivity, ease of cell harvesting and biomasscomposition manipulation [8]. The surface of A. platensis consistsof various macro-molecules with diverse functional groups such ascarboxyl, hydroxyl, sulphate and phosphate, which are responsiblefor dye binding [9]. A. platensis has already been studied for theremoval of inorganic pollutants such as heavy metals [6,10–12] andorganic pollutants such as anionic dyes [9,13–15] and phenol[16,17] from aqueous solutions. To our knowledge, there is lack ofpublished work about the adsorption of cationic dyes onto A.

* Corresponding author. Tel.: +30 6974876236.E-mail address: mitrogiandimi@yahoo.gr (D. Mitrogiannis).

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Journal of Environmental Chemical Engineering 3 (2015) 670–680

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platensis. The only related study to this, uses an artificial neuralnetwork to predict the biosorption capacity of methylene blue ontoSpirulina sp. [18]. However, there is no literature information aboutthe biosorption kinetics and thermodynamics of a cationic dye onthis cyanobacterium and about the contribution of the ionexchange mechanism on dye removal. Although the importantrole of the ion exchange mechanism in MB removal by variousbiosorbents is mentioned very often, it has not been widelyinvestigated by detection measures [7].

Methylene blue (MB) is a common cationic dye used for dyeingpaper, cotton, wool and silk [7,19]. The harmful effects of MBinclude: breathing difficulties, nausea, vomiting, tissue necrosis,profuse sweating, mental confusion, cyanosis and methemoglobi-nemia [5,7]. MB has been widely employed as a model cationic dyein adsorption studies, using low-cost adsorbents such as naturalminerals (clays, zeolites and perlite), activated carbon, dead ornon-growing microbial biomass, agricultural and industrial wastes[7].

The aim of the present study was to investigate the potential ofA. platensis dry biomass to remove MB dye from aqueous solutions.The effect of solution pH, initial MB concentration, contact time,temperature and ionic strength on the biosorption capacity wasinvestigated. Kinetic, isotherm and thermodynamic parameterswere estimated to understand the biosorption rate and mecha-nisms of MB onto A. platensis.

Materials and methods

Biosorbent cultivation and preparation

The cyanobacterium A. platensis (SAG 21.99) used in this studywas cultivated in Zarrouk medium within 10 L plastic cubicalphotobioreactor, which were kept at 303 � 2 K in semi-continuouscultivation mode with a dilution rate of 0.11/d [6]. The A. platensisbiomass was harvested by filtration and rinsed with deionized (DI)water. The cultivation medium salts were removed by washing thebiomass twice by re-suspension in DI water. After that the biomasswas separated with centrifugation (5000 rpm for 5 min) and driedovernight in an oven at 353 K. The dried biomass was milled (IKALabortechnik, A10), sieved through a metal sieve (100 mesh,particle diameter <154 mm), and stored in a plastic containerinside an exsiccator containing silica gel to prevent moisturesorption by the biomass. The chemical composition of the driedbiomass consisted of 45–55% proteins, 10–20% carbohydrates, and5–7% lipids [6].

Preparation of dye solution

MB is a cationic dye with molecular formula C16H18N3SCl andmolar weight of 319.85 g/mol. This cationic dye presents highwater solubility at 293 K and is positively charged on S atom [20].MB stock solution (1 g/L) was prepared by dissolving an appropri-ate weighed amount of MB hydrate reagent (analytical grade,Sigma–Aldrich, India) in 1 L DI water. The experimental solutions ofdesired initial concentrations were obtained by dilution of MBstock solution with DI water.

Determination of pH zero point charge of A. platensis

To determine the zero point charge (pHzpc) of A. platensisbiomass, the initial pH of 25 mL solutions containing 0.5 g/L ofbiosorbent and 0.1 M NaCl was adjusted at pH values ranging from3 to 9, using 0.1 M HNO3 and/or NaOH [19,20]. The samples wereagitated for 24 h at 298 K, and the final pH values were measuredusing a pH-meter (Consort P603, Belgium). Value of pHzpc wasdetermined from the plot of final pH against initial pH.

Batch biosorption experiments

The biosorption experiments were carried out in batch mode bymixing 12.5 mL aqueous suspension containing 12.5 mg driedbiomass with 12.5 mL MB dye solution of known concentration.The final 25 mL solution was placed in a 50 mL plastic flask, whichwas sealed and agitated with a rotary shaker at 140 rpm. Thedesired initial pH (range 4–10) of the adsorbate and adsorbentsolution was adjusted using 0.1 M HNO3 and/or NaOH beforemixing them.

Biosorption kinetics were investigated with a biomass concen-tration of 0.5 g/L at three initial dye concentrations (25, 50 and100 mg/L) and pH 7.5 � 0.1. Samples were collected at timeintervals (2, 5, 10, 15, 30, 60, 90, 120, 180 and 240 min) andsubjected to MB concentration determination. The kinetic experi-ments were conducted in an air-conditioned room with tempera-ture of 298–300 K. Equilibrium experiments were carried out at298, 308 and 318 K, placing the flasks and shaker in a temperaturecontrolled incubator and using five different initial MB concen-trations (6.25, 12.5, 25, 50 and 100 mg/L), in order to estimate theparameters of isotherm models and thermodynamic equations.The contact time of equilibrium experiments was chosen to be24 h.

The amount of MB adsorbed per unit weight of A. platensisbiomass at equilibrium, qe (mg/g), and the percentage dye removal(R%), were calculated with the following equations:

qe ¼ðC0 � CeÞ

X(1)

R ¼ 100ðC0 � CeÞC0

(2)

where C0 (mg/L), Ce (mg/L) and X (g/L) are the initial MBconcentration, the MB concentration at equilibrium, and thesorbent concentration in the solution, respectively.

The effect of ionic strength on the biosorption capacity wasstudied in solution containing 0.5 g biosorbent/L, 50 mg MB/L and0.0625–0.5 M NaCl at optimum pH (7.5). For the investigation ofthe possible ion exchange mechanism involved in the biosorptionprocess, the concentrations of cations Na+ and K+ released from thebiomass after MB sorption were determined. Biomass of 0.5 g/Lwas added in 50 mL solution containing either DI water or 100 mgMB/L, which was shaken for 24 h at 298–318 K. The initial pH of thedye solution was adjusted at 7.5 � 0.1 using dilute NH4OH and HClsolutions. The cations released in the 0 mg MB/L solutioncontaining only dried biomass were considered as backgroundconcentration, which was subtracted from the cation amountreleased after MB sorption in order to calculate the net cationrelease. Blank solution of 100 mg MB/L was also used to confirm nopresence of cations.

Chemical modification of carboxyl groups on the biomass surface

The chemical modification of the dried biomass was applied tounderstand the role of the surface carboxyl groups in MB sorption.The aim of the modification was to block the carboxyl groups byesterification and then to determine the decrease of biosorptioncapacity. The esterification of the dried biomass was carried outaccording to the method described by Fang et al. [21]. 1.0 g driedbiomass of A. platensis was suspended in 50 mL of 99.9% methanolsolution and 0.6 mL concentrated HCl. The suspension was agitatedfor 48 h at 333 K and allowed to cool at room temperature. Themodified biomass was washed three times by re-suspension in DIwater. After that the biomass was separated with centrifugation(5000 rpm for 5 min) and dried overnight in an oven at 323 K. For

D. Mitrogiannis et al. / Journal of Environmental Chemical Engineering 3 (2015) 670–680 671

the biosorption study, 100 mg of modified dried biomass weresuspended in 100 mL DI water and homogenized with ahomogenizer (IKA-Labortechnick, Ultra Turrax T10, Germany).Then 12.5 mL modified biomass suspension was mixed with12.5 mL solution of 200 mg MB/L. The final 25 mL solutioncontaining 100 mg MB/L and 0.5 g/L of chemically modifiedbiosorbent was agitated for 24 h at 298 K and pH 7.5. The sameprocedure was done for the untreated dried biomass of A. platensisfor comparison purpose.

Analytical methods

For the determination of the unadsorbed MB concentration ineach solution, 0.5 mL of sample was withdrawn at the preselectedtime, t, and was placed in an Eppendorf type centrifuge tube(1.5 mL), which contained 1 mL DI water. The diluted sample wascentrifuged for 2 min at 10,000 rpm. The supernatant wascollected, diluted with appropriate DI water, and the MBconcentrations were determined at the wavelength of 665 nmusing a UV–vis spectrophotometer (Dr. Lange, Cadas 30, Germany).The concentrations of Na+ and K+ were determined with a flamephotometer (Sherwood Scientific, model 400), followed byseparation of the biomass from the sorption solution bycentrifugation at 10,000 rpm for 5 min. All experiments wereperformed in triplicates and the average values were recorded.

Mathematical models

Kinetic modelsThe biosorption kinetic experimental data were fitted with the

following models:The pseudo-first order model expressed by the following

linearized form [4]:

log qe � qtð Þ ¼ logqe �k1

2:303

� �t (3)

where qe (mg/g) and qt (mg/g) are the amount of adsorbed dye pergram of biomass at equilibrium and at time t, respectively, and k1(1/min) is the pseudo-first order rate constant.

The pseudo-second order model expressed by the followinglinearized form [4]:

tqt

¼ 1kzqze

þ tqe

(4)

where k2 (g/mg min) is the pseudo-second order rate constant.The intra-particle diffusion model of Weber–Morris expressed

by the following equation [6]:

qt ¼ kidt0:5 þ I (5)

where kid (mg/g min0.5) is the intra-particle diffusion rate constant,and I (mg/g) is the y-intercept which reflects the boundary layerthickness.

Equilibrium isotherm modelsThe biosorption equilibrium data were applied to the following

isotherm models:The Langmuir isotherm expressed by the following linearized

form [22]:

1qe

¼ 1qmax

þ 1qmaxKLCe

(6)

where qmax (mg/g) is the maximum monolayer adsorptioncapacity, and KL (L/mg) is the Langmuir isotherm constant relatedto the affinity and binding energy. The constant KL is used for theprediction of the affinity between sorbate and biosorbent by thedimensionless separation factor, RL, which is defined as [23]:

RL ¼ 11 þ KLC0

(7)

where C0 (mg/L) is the initial dye concentration.The Freundlich isotherm expressed by the following linearized

form [24]:

lnqe ¼ lnKF þ 1nlnCe (9)

where KF [(mg/g) (L/g)1/n] is the Freundlich isotherm constantrepresenting the adsorption capacity, and n is a dimensionlessfactor related to adsorption intensity and surface heterogeneity.

The Dubinin–Radushkevich (D–R) isotherm expressed by thefollowing linearized form [24]:

lnqe ¼ lnqs � KDR RTln 1 þ 1Ce

� �� �2(9)

where qs (mol/g) is the theoretical isotherm saturation capacity,KDR (mol2/kJ2) is the Dubinin–Radushkevich isotherm constant, R(8.314 J/mol K) is the gas constant, and T (K) the absolutetemperature.

Goodness of model fitThe fit goodness of the applied mathematical models to the

experimental data was determined by the following threeprocedures: (1) the coefficient of determination (R2) to thelinearized data (linear regression), (2) the composite fractionalerror function (CFEF) and (3) the chi-square statistic (x2). The lasttwo non-linear functions, which measure the difference betweenexperimental and model predicted data, can be expressed by thefollowing equations [6]:

CFEF ¼Xnn¼1

ðqe;exp � qe;calÞ2qe;exp

" #(10)

x2 ¼Xnn¼1

ðqe;exp � qe;calÞ2qe;cal

" #(11)

where qe,exp (mg/g) and qe,cal (mg/g) are the experimental andmodel calculated values of adsorption capacity, respectively, and nis the number of experimental samples. The smaller the values ofCFEF and x2, the more similar are the calculated data to theexperimental one.

Results and discussion

Effect of initial solution pH

Fig. 1a shows the plot of initial pH versus final pH, wherein thepHzpc value (6.8) of A. platensis was determined by the intersectionpoint of both curves. This pHzpc value is very similar with thatreported in other studies [13,15,23] which found a pHzpc 7 forSpirulina platensis using the method of the eleven pointsexperiment [15,23]. At pHzpc the biosorbent surface is neutral.

The initial pH of the sorption solution is one of the mostimportant factor of adsorption process affecting the surface chargeof the biosorbent and the ionization of the dye [3]. The surfacecharge distribution of a biosorbent depends on the kind andquantity of functional groups, and the solution pH [25]. Fig. 1bshows the effect of initial pH on the MB biosorption onto A.platensis at equilibrium (24 h). It was observed that qe increased asinitial pH of the solution increased from 4 to 8, and then decreasedat pH values of 9 and 10. Therefore, the initial pH of sorptionsolutions for the following experiments was adjusted to 7.5 � 0.1.

At pH > pHzpc the biosorbent surface is negatively charged dueto the deprotonation of functional groups such as carboxyl, amino,

672 D. Mitrogiannis et al. / Journal of Environmental Chemical Engineering 3 (2015) 670–680

phosphate and hydroxyl [13,21], and thus electrostatic attractioncan occur between the negatively charged functional groups ofbiosorbent surface and the positively charged cationic dye [11]. Incontrast, at pH < pHzpc the biosorbent surface is positively chargedand electrostatic repulsion occurs between MB cations and A.platensis surface. At acidic pH, the H+ ions compete with MB cationsfor available binding sites onto A. platensis [3]. However, theremarkable qe at pH < pHzpcwhere the most of the binding sites areprotonated, suggests that hydrophobic interactions also contrib-uted to MB removal [26]. In addition, based on typical deproto-nation constants for short chained carboxylic groups (4 < pKa< 6),the increased MB binding in the pH range of 4–6 may be alsoattributed to the deprotonation of carboxyl groups [21]. This wasconfirmed by the chemical modification of dried cells and theesterification of surface carboxyl groups, which resulted to thedecrease of the biosorption capacity (see Biosorption mecha-nisms).

The decrease of qe at pH > 8 is difficult to be explained. Similarresult was observed at pH 9.5–11 for MB adsorption on cedarsawdust [27]. Some of the reasons for the biosorption decrease athigh pH values might be the involvement of other adsorptionmechanisms such as ion exchange or chelation, or the hydrolysis ofthe biosorbent surface which creates positively charged bindingsites [27]. In this study, it was observed that the equilibrium pH(pHe) of the samples at initial pH 9 and 10 decreased by 0.85–1.23 units, indicating that an exchange mechanism of H+ ions withMB cations occurred (Fig.1b). However, other dye–dye interactionssuch as an increased formation of MB aggregates at higher pH,which are unable to enter into the pores of A. platensis, may beresponsible for the decreased qe at pH 9 and 10 [28].

Biosorption kinetics

Biosorption kinetic experiments were carried out at three initialMB concentrations and at temperature of 298 K. As shown inFig. 2a, the biosorption of MB onto A. platensis was very rapid in thefirst 2–10 min for all studied concentrations. After the rapidadsorption during the initial stage, the biosorption increased at aslower rate with time and equilibrium was established within 60–120 min for all initial MB concentrations. Equilibrium capacity didnot change significantly up to 24 h (data not shown). Theequilibrium time is in agreement with a previous work aboutMB biosorption by Spirulina sp. [18].

The pseudo-first order model could not describe the kineticdata, because the plot of log (qe� qt) versus t (Eq. (3)) presentedvery low values for R2 (<0.355) at all initial dye concentrationsinvestigated. Therefore, the kinetic parameters of this model arenot shown in Table 1.

The kinetic parameters qe and k2 of the pseudo-second ordermodel, obtained from the linear plots of t/qt versus t (Eq. (4)), andthe values of error functions are listed in Table 1. Based on thelinear regression analysis of the kinetic data (Fig. 2b), the pseudo-second order model described very well the overall experimentaldata with R2 > 0.988. The applicability of this model suggests thatthe biosorption rate was controlled by chemisorption [29],involving exchange or sharing of electrons between the MBcations and functional groups of the biomass surface [30]. For the

Fig. 1. (a) Plot of initial pH versus final pH for the determination of biomass pHzpc,and (b) the effect of initial pH on MB biosorption onto A. platensis (pHe = equilibriumpH).

Fig. 2. (a) Effect of contact time on MB biosorption onto A. platensis at threedifferent initial MB concentrations (biomass dosage = 0.5 g/L, pH 7.5, temperature =298 K). Symbols and curves represent the experimental data and the fitted pseudo-second order kinetic model, respectively. (b) Pseudo-second order model linearplots for MB biosorption onto A. platensis biomass.

D. Mitrogiannis et al. / Journal of Environmental Chemical Engineering 3 (2015) 670–680 673

pseudo-second order kinetics, the calculated qe values (qe,cal)agreed well with the experimental q values (qe,exp) (Table 1).However, the nonlinear analysis of the kinetic data for the initialMB concentration of 50 mg/L showed relative high CFEF and x2

values (Fig. 2a), which are due to an underestimation of the earlytime data (first 30 min) by the kinetic model [6].

The biosorption capacity (qe) at equilibrium, calculated fromthe pseudo-second order model, increased with increasing initialMB concentration (Table 1). However, the pseudo-second orderrate constant (k2) decreased slightly when the initial MBconcentration increased from 25 to 100 mg/L, but its values[0.0134–0.0247 g/(mg min)] demonstrated a same magnitude forall studied concentrations (Table 1). A decreasing value of k2suggests that the biosorption equilibrium capacity was establishedslower at higher MB concentrations due to the limited quantity ofbinding sites at the biosorbent surface [25]. In addition, thenonlinear relationship between the rate constant values and initialMB concentrations suggest that various mechanisms involved inthe biosorption process, such as ion exchange, chelation andphysisorption [31].

The initial adsorption rate h (mg/g min) at 298 K was calculatedfrom the pseudo-second order model parameters with thefollowing equation [32]:

h ¼ k2q2e (12)

and the values are shown in Table 1. It was found, that the initialadsorption rate h increased from 18.52 to 138.89 mg/(g min) as theinitial MB concentration increased from 25 to 100 mg/L. This resultsuggests an increasing driving force between the liquid and thesolid phase at higher dye concentrations and a decreasing diffusiontime of MB molecules from the solution to the binding sites [26].This observation is in agreement with previous findings reportedfor MB adsorption on coconut bunch waste (Cocos nucifera) [32]and marine algae Gelidium [26].

The half adsorption time or half-life, t0.5 (min), expresses thetime required for the biosorbent to remove the adsorbed amount ofdye at equilibrium to its half, and is calculated from the pseudo-second order model parameters with the following equation [33]:

t0:5 ¼ 1ðk2qeÞ

(13)

As shown in Table 1, the estimated values of t0.5 decreased from1.479 to 0.581 min when the initial MB concentration increased,indicating a faster biosorption [33]. This parameter is used as ameasure of adsorption rate and to understand the operating timeof an adsorption system [33].

Fig. 3 shows the behavior of the intra-particle diffusion modelof Weber–Morris at three initial MB concentrations and 298 K. Thismodel was applied to the kinetic data in order to determine thebiosorption process mechanism and the rate controlling step. Asshown in Table 1, the values of R2 obtained from the linearregression plots of qt versus t0.5 for the whole time data of thesorption process, were low (<0.583). The low R2 values suggestthat the Weber–Morris model could not describe well theexperimental data and that the MB biosorption process was notlimited by the intra-particle diffusion. However, the calculatedCFEF and x2 values were very low (Table 1), suggesting that thismodel fits well the experimental data for the overall time data. Tothe best of our knowledge, there is no report known in literatureabout the intra-particle diffusion analysis of kinetic data forcationic dyes onto A. platensis.

At all studied concentrations, the plot of qt versus t0.5 consists ofthree linear sections, which do not pass through the origin (I 6¼ 0). IfI = 0, then the intra-particle diffusion is the sole rate-limiting step.The multi-linearity of the plots suggests also that MB biosorptiononto A. platensis biomass took place in three phases. The first steepersection represents the external mass transfer (film diffusion) of dyeto biosorbent surface [13], which was completed very fast in the first2–5 min of the process. The second linear section (completed up to90–120 min) describes a gradualsorptionstagewhere intra-particlediffusion is the rate-controlling step [34]. The third linear section(starting after 120 min) represents the final equilibrium stage,where intra-particle diffusion starts to slow down and an apparentsaturation occurs [13,34].

The high values of R2 (0.944 and 0.961 respectively) obtainedfrom the second linear sections of the intra-particle diffusion plotat initial dye concentrations of 50 and 100 mg/L, indicate that intra-particle diffusion occurred during this phase (Fig. 3,Table 1). Asshown in Table 1, the intra-particle diffusion rate constant, kid,2,

Table 1Kinetic and diffusion model parameters for MB biosorption onto A. platensis.

Initial dye concentration (mg/L)

25 50 100

qe,exp (mg/g) 29.48 54.94 82.95

Pseudo-first order modelR2 0.355 0.241 0.337

Pseudo-second order modelqe,calc (mg/g) 27.40 55.56 80.65k2 (g/mg min) 0.0247 0.0134 0.0214h (mg/g min) 18.52 41.32 138.89t0.5 (min) 1.479 1.344 0.581R2 0.998 0.998 0.988CFEF 3.46 18.49 6.39x2 4.84 29.36 6.40

Intra-particle diffusion model:Whole time datakid (mg/g min0.5) 0.307 0.197 1.220I (mg/g) 23.25 59.11 67.66R2 0.583 0.269 0.517CFEF 0.52 0.39 3.88x2 0.54 0.39 3.70

Intra-particle diffusion model:Second linear sectionkid,2 (mg/g min0.5) 0.562 1.024 2.866I (mg/g) 22.05 54.59 58.94R2 0.646 0.944 0.961CFEF 0.48 0.15 0.94x2 0.50 0.15 0.91

Fig. 3. Intra-particle diffusion of MB cationic dye onto A. platensis at three differentinitial MB concentrations and 298 K.

674 D. Mitrogiannis et al. / Journal of Environmental Chemical Engineering 3 (2015) 670–680

estimated from the slope of the second linear section (Fig. 3),increased from 0.562 to 2.866 mg/(g min0.5) with the increasinginitial dye concentration from 25 to 100 mg/L. This observationshows a faster intra-particle diffusion at higher initial concen-trations [16]. For the same linear section, the values of they-intercept I increased from 22.05 to 58.94 mg/g when the initialMB concentration increased. This result indicates an increasingboundary layer effect and a greater involvement of the filmdiffusion at higher dye concentrations, for this particular timerange. Similar results for kid and I were observed for thebiosorption of phenol on S. platensis nanoparticles [16].

Effect of initial MB concentration and temperature

Fig. 4 illustrates the effect of the initial MB concentration on theequilibrium biosorption capacity of A. platensis at differenttemperatures. It was observed that qe increased with the increaseof initial MB concentration at all temperatures studied. At 298 K,the amount of MB adsorbed was 7.55 mg/g for the lowest initial MBconcentration of 6.25 mg/L and increased to 89.56 mg/g for thehighest initial MB concentration of 100 mg/L. This observation canbe explained by the increasing driving force which overcome themass transfer resistance of MB dye between the aqueous and solidphase [1,4]. Further, the number of collisions between MB cationsand biosorbent can be increased due to the increasing initial dyeconcentration, enhancing the sorption process [4]. The increasingdriving force at higher dye concentrations is in agreement with theabove mentioned results for the initial adsorption rate h (at 298 K),which is estimated by the parameters of the pseudo-second orderkinetic model.

Although the enhancement of MB biosorption at higher initialdye concentrations was also observed at 308 and 318 K, the valuesof qe for each initial concentration decreased with the increasingsolution temperature (Fig. 4). According to Dotto et al. [23], thesolubility of the dyes increases due to the temperature increase. Asa result, the interactions between MB molecules and the solventare stronger than those between MB and A. platensis. As shown inFig. 4, the qe for the highest initial MB concentration of 100 mg/L,decreased from 89.56 mg/g at 298 K to 82.18 and 65.70 mg/g at308 and 318 K, respectively. These results suggest the exothermicnature of MB sorption process and a mechanism of physicalsorption, dominant at lower temperatures [4]. These findings arefurther discussed by the thermodynamics analysis of isothermexperimental data in Biosorption thermodynamics.

The effect of the initial MB concentration on the percentageremoval at different temperatures is shown in Fig. 4. Thepercentage removal of MB at 298 K decreased from 60.4 to44.8% when the initial dye concentration increased from 6.25 to100 mg/L. The same tendency of a decreasing percentage removal

of MB was observed at 308 and 319 K. The only exception was theincrease of percentage removal between the two lowest initial MBconcentrations of 6.25 and 12.5 mg/L at all temperatures studied.The negative effect of the increasing initial dye concentration onthe percentage removal may be due to the saturation of theadsorption sites at higher MB concentrations [5]. Similar resultswere observed for the MB adsorption onto acid treated kenaf fiberchar [5].

Biosorption isotherms

The relationship between the adsorbate (dye) concentration inthe liquid phase and the adsorbed dye amount per unit weight ofbiosorbent at equilibrium was analyzed using three commonisotherm models.

The calculated values of the adsorption isotherm parametersand error functions for MB biosorption onto A. platensis are listed inTable 2. Based on the R2 values, the Dubinin–Radushkevich modelwhich was mainly used to investigate the MB sorption mechanism,exhibited the best fit to the experimental data at all studiedtemperatures (R2 > 0.963). Although the Langmuir and Freundlichisotherm models presented satisfactory and similar determinationcoefficients (R2 > 0.950 and 0.960, respectively), the Freundlichmodel could better describe the experimental data than theLangmuir model due to the lower CFEF and x2 values (Table 2).

Thus, the good and similar agreement of the three appliedisotherm models with the experimental data show that the MBsorption was a complex process, involving more than onemechanism [4]. Both the monolayer biosorption and surfaceheterogeneity of biosorbent affected the removal of MB from thesolution [4], and no clear biosorption saturation was occurred inthe studied range of MB concentration [34].

0

20

40

60

80

100

0

20

40

60

80

100

6.25 12.5 25 50 10 0

MB

Rem

oval

(%)

q e(m

g/g)

C0 (mg/ L)

298 K

308 K

318 K

R% 2 98 K

R% 3 08 K

R% 3 18 K

Fig. 4. Effect of initial MB concentration on the percentage removal of MB and thebiosorption capacity of A. platensis at different temperatures.

Table 2Isotherm parameters values of MB biosorption onto A. platensis at differenttemperatures.

Solution temperature (K)

298 308 318

qe,exp (mg/g) 89.56 82.18 65.70

Langmuirqmax (mg/g) 312.50 204.08 80.65qe,cal (mg/g)a 117.42 86.94 59.31KL (L/mg) 0.0109 0.0126 0.0414RL (range) 0.478–0.936 0.442–0.927 0.195–0.794R2 0.950 0.989 0.952CFEF 10.82 4.02 3.71x2 8.96 3.24 3.62

Freundlichqe,cal (mg/g)a 99.75 82.55 64.95KF ((mg/g) (L/mg)1/n) 4.766 3.512 5.003n 1.319 1.291 1.641R2 0.967 0.981 0.960CFEF 2.86 1.50 1.42x2 2.89 1.50 1.59

Dubinin–Radushkevichqs (mol/g) 0.0048 0.0042 0.0017BD (mol2/kJ2) 6.05 �10�9 5.85 �10�9 4.31 �10�9

E (kJ/mol) 9.09 9.25 10.77R2 0.974 0.986 0.963CFEF 4.98 � 10�6 4.73 �10�6 4.93 �10�6

x2 5.42 � 10�6 4.46 � 10�6 5.40 � 10�6

a qe,cal corresponds to C0 = 100 mg/L.

D. Mitrogiannis et al. / Journal of Environmental Chemical Engineering 3 (2015) 670–680 675

The Langmuir model assumes a monolayer adsorption ontohomogeneous surfaces with finite number of binding sites and nointeraction between adsorbate molecule [1,4]. The constants qmax

and KL were estimated from the intercept and slope of the linearplot of experimental data of 1/qe versus 1/Ce (Fig. 5a).

The maximum monolayer adsorption capacity (qmax) decreasedfrom 312.50 to 80.65 mg/g when the temperature increased from298 to 318 K (Table 2). However, the Langmuir constant KL

increased with the increasing temperature (Table 2), indicatinga higher affinity (0.0414 L/mg) of A. platensis biomass for the MB

molecules at 318 K. The values of the dimensionless separationfactor, RL, found to be less than unity and greater than zero(0 < RL< 1) at all initial MB concentrations and temperatures,confirming a favorable sorption process. If RL > 1 the adsorption isunfavorable. As shown in Fig. 6, the higher the initial MBconcentration, the lower the RL value and the more favorablethe MB biosorption.

A comparison of the maximum monolayer adsorption capacity(qmax) for MB onto various adsorbents [25,26,35–38] and thatobtained onto A. platensis in this work, shows that the cyanobacte-rium is an efficient biosorbent for the removal of MB from aqueoussolutions. According to recent studies, S. platensis presented also asatisfactory biosorption capacity for anionic dyes [9,13,23,39].

The Freundlich model assumes a multilayer adsorption ontoheterogeneous surfaces with energetically non-equivalent bindingsites and interactions between adsorbent molecules [1]. Theconstants KF and n were evaluated from the intercept and slope ofthe linear plot of experimental data of ln (qe) versus ln (Ce) (Fig. 5b).

The values of the dimensionless Freundlich constant n relatedto the adsorption intensity and surface heterogeneity, were higherthan 1 and less than 10 (1 < n < 10) (see Table 2), indicating afavorable sorption of MB onto A. platensis biomass at all studiedtemperatures. No significant difference for n values was observedwith respect to temperature. The parameter KF represents arelative measure of adsorption capacity and strength. When theequilibrium concentration Ce tends to be one, then KF reaches thevalue of qe [4]. As can be seen in Table 2, the values of KF increasedslightly with the rising temperature from 298 to 318 K, butdecreased between 298 and 308 K. It shows that the multilayerbiosorption of MB was enhanced at higher solution temperature.

To distinguish between physical and chemical sorption, themean free energy E (kJ/mol) of MB biosorption was calculated bythe following equation:

E ¼ 1ffiffiffiffiffiffiffiffiffiffiffi2KDR

p (14)

where KDR (mol2/kJ2) is the constant of Dubinin–Radushkevichisotherm.

The parameter E is related to the mean free energy of sorptionper molecule of sorbate, assuming that the sorbate is transferred tothe biosorbent surface from infinite distance in the solution.Typical values of E for chemical sorption are in the range of 8–16 kJ/mol, while E < 8 kJ/mol indicates physical sorption [24]. As shownin Table 2, the mean free energy E of MB biosorption onto A.platensis suggests a chemisorption mechanism, because its valuesare in the range of 8–16 kJ/mol at all studied temperatures. Theincreasing temperature caused a slight increase of E from 9.09 to10.77 kJ/mol, indicating an enhancement of the chemisorption athigher temperatures. The biosorption mechanisms are furtherdiscussed in Biosorption mechanisms.

Biosorption thermodynamics

The thermodynamic behavior of MB biosorption onto A.platensis biomass was investigated estimating the thermodynamicparameters of Gibbs free energy change (DG�), enthalpy change(DH�) and entropy change (DS�). The values of these parameterswere estimated using the following equations [35]:

DG� ¼ �RTlnKc (15)

DG� ¼ DH� � TDS� (16)

Fig. 5. Linear plots of (a) Langmuir and (b) Freundlich isotherm model for the MBbiosorption onto A. platensis at different temperatures.

Fig. 6. Relationship between initial MB concentration and dimensionless separa-tion factor RL at different temperatures.

676 D. Mitrogiannis et al. / Journal of Environmental Chemical Engineering 3 (2015) 670–680

lnKc ¼ DS�

R�DH�

RT(17)

where R is the universal gas constant [8.314 J/(mol K)], T theabsolute solution temperature (K), and Kc (Cad,e/Ce) is theadsorption equilibrium constant, which is the ratio of the MBconcentration adsorbed (Cad,e) to the MB concentration (Ce) insolution at equilibrium [38].

The negative values of DG� indicates a spontaneous andfavorable adsorption process at all studied temperatures andinitial concentrations (see Table 3), suggesting that the systemrequired no energy input from outside [23]. Similar thermody-namic behavior in respect to negative DG� values has been foundfor S. platensis dry biomass as a biosorbent of anionic dyes[13,23,39]. For a given initial MB concentration in this work, nosignificant change of DG� was observed with increasing tempera-ture. However, the DG� values decreased slightly as the initial MBconcentration increased from 50 to 100 mg/L, indicating a morefavorable adsorption of MB at lower dye concentration.

The values of enthalpy change (DH�) and entropy change (DS�)can be calculated from the slope and intercept of the linear plot ofln Kc versus 1/T, based on the Eq. (17). As shown in Fig. 7, thedetermination coefficient (R2) of the plots was 0.939 and 0.940 forthe two highest initial MB concentrations, respectively, indicatingthat the estimated values of DH� and DS� were confident. As can beseen in Table 3, the negative values of DH� at all studied initial dyeconcentrations correspond to an exothermic nature of MBbiosorption. Similar results for the cyanobacterium in respect tonegative DH� values obtained by other studies, which found anexothermic biosorption of anionic dyes [13,23,39] and phenol [17]onto S. platensis dry biomass.

There are different results in the literature in respect to theexothermic or endothermic nature of MB adsorption onto variousmaterials, based on the estimated DH� values. An exothermicadsorption of MB was found onto cyclodextrin/silica hybridadsorbent [38] and green algae Ulothrix sp. [31]. On the otherhand, an endothermic adsorption of MB was found onto diatomitetreated with sodium hydroxide [29], marble dust [19], montmo-rillonite clay [1], and acid treated kenaf fiber char [5].

The magnitude of enthalpychange can be used to classify the typeof interaction between sorbent and sorbate. Values of DH� < 30 kJ/mol indicates a physical sorption such as hydrogen bonding [13].Other mechanisms of physical sorption such as van der Waals forcesusually presents DH� values in the range 4–10 kJ/mol, hydrophobicbonds forces about 5 kJ/mol, coordinationexchange about 40 kJ/moland dipole bond forces 2–29 kJ/mol [13]. In contrast, DH� > 80 kJ/mol indicates chemical bond forces and a chemisorption process[13,17,20]. According to the DH� values (<28.32 kJ/mol) obtained inthis study, the biosorption of MB dye onto A. platensis biomass wasdue to physical adsorption, suggesting weak interactions betweenbiomass and cationic dye [38]. Further, the negative effect ofincreasing temperature on qe (Fig. 4) and the applicability of thepseudo-second order kinetic model showed that MB sorptionprocess involved both mainly physical and partly chemical sorption[4]. The low negative values of DG� ranging from �20 to 0 kJ/mol

suggest that the dominant biosorption mechanism was physisorp-tion [1].

The weak binding and weak interactions between thebiosorbent and the adsorbate showed that the adsorbed MBmolecules should be easily released [38]. This point should befurther investigated in order to evaluate the regeneration andreuse ability of A. platensis after dye desorption, in order to reducethe cost of the biosorption process.

The negative values of DS� for 50 and 100 mg MB/L were verylow, indicating no remarkable change on entropy [36] and adecreased disorder at the solid–liquid interface during the MBbiosorption onto A. platensis (see Table 3). This showed also thatthe dispersion degree of the process decreased with increasingtemperature [35]. Based on the Eq. (16) and the differentmagnitude of DH� and DS� values (Table 3), the enthalpy change(DH�) contributed more than entropy change (DS�) to obtain thenegative values of DG� [23]. This observation suggests that MBbiosorption onto A. platensis was an enthalpy-controlled process[39].

Effect of ionic strength

Dye effluents contain high concentrations of salts which affectthe dye sorption onto biosorbents. Fig. 8 presents the effect of ionicstrength on the MB biosorption by A. platensis at 298 K and pH 7.5.It was observed that qe decreased as the NaCl concentration insorption solution increased from 0.0625 to 0.5 M. The decrease of

Table 3Thermodynamic parameters of MB biosorption onto A. platensis biomass.

C0(mg/L)

DH�

(kJ/mol)DS�

(kJ/mol/K)DG� (kJ/mol)

298 K 308 K 318 K

50 �28.32 �0.036 �17.65 �16.89 �16.94100 �19.81 �0.011 �16.60 �16.77 �16.37

Fig. 7. Plots of ln Kc versus 1/T for the estimation of thermodynamic parameters ofMB biosorption onto A. platensis.

0

10

20

30

40

50

60

0 0. 1 0. 2 0. 3 0. 4 0. 5 0. 6

q e(m

g/g)

NaCl (mol/L)

Fig. 8. Effect of ionic strength on MB biosorption onto A. platensis (C0 = 50 mg MB/L,pH 7.5, temperature = 298 K).

D. Mitrogiannis et al. / Journal of Environmental Chemical Engineering 3 (2015) 670–680 677

qe is due to the competitive effect between Na+ and MB cations forthe available surface binding sites [36] and the electrostaticallyscreening effect of salt [40]. The latter indicates that theelectrostatic interactions should be one of the main driving forcesduring MB biosorption process [40]. However, the remarkablebiosorption capacity observed even in the presence of much higherNaCl concentration (62.5 mmol/L) than the initial MB concentra-tion of 50 mg/L (= 0.156 mmol/L) suggests that other interactionssuch as hydrophobic interactions, p–p interactions and/orhydrogen bonding, contributed to MB removal [40].

Biosorption mechanisms

The amounts of Na+ and K+ cations released from A. platensissurface into the solution after MB sorption are listed in Table 4.Based on the total net cations release at 298 K, it is evident that thecation exchange was one of the major biosorption mechanisms atthis temperature. In contrast, the net cations release at highertemperatures was negligible. Besides, no significant changebetween initial and equilibrium pH was observed at all studiedtemperatures (Table 4), suggesting that ion exchange between MBcations and protons (H+) of surface functional groups did not takeplace at pH 7.5. A previous study has confirmed the presence of Na+

and K+ on the cell wall surface of Spirulina sp. [41]. The total releaseof both cations measured in mg/L (data not shown) constituted upto 4.7% of the dried biomass weight (500 mg/L), which agrees withthe ash percentage (6.3–7%) in the chemical composition of S.platensis dried biomass reported in the literature [9,39]. Themechanism of cation exchange between MB molecule andthe exchangeable cations of biomass surface can be describedby the following equations [42]:

S—O—K + CN+! S—O—CN + K+ (18)

S—O—Na + CN+! S—O—CN + Na+ (19)

where S is the surface of A. platensis biomass, Na+ and K+ are theexchangeable cations, and CN+ is the positively charged nitrogenatom of the secondary amine group of MB molecule.

Fig. 9 shows the effect of the chemical modification of carboxylgroups on the biosorption capacity. The esterified biomass of A.platensis presented a decrease in the MB biosorption capacity(62.66 mg/g) by 25.5% compared to the biosorption capacity of theuntreated biomass (83.83 mg/g) (Fig. 9), due to the block of thesurface carboxyl groups. This result indicated the participation ofcarboxyl groups in the MB binding by the untreated biomass,which is a chemisorption process. The cell wall of cyanobacteriacontains a thick structural layer of peptidoglycan and an extended

layer of glycoproteins and polysaccharides. These layers are themain source of reactive carboxyl groups on the biosorbent surface[21]. The reaction of the chemical esterification of surface carboxylgroups is described by the following equation, where R are all thecomponents in the dried cells [21]:

RCOOH + CH3OH ! RCOOCH3 + H2O (20)

Recent studies for the removal of anionic dyes from aqueoussolutions confirmed the mesoporous structure of S. platensis driedmicroparticles which presented a particle size in the range of 68–75 mm and an average pore radius of 2.25 nm (22.5 Å) [9,13]. Notethat the average pore radius was not modified even in case of S.platensis nanoparticles obtained from the microparticles through amechanical method [9]. Therefore, the A. platensis microparticles(with particle diameter <154 mm) employed in this study mighthave a mesoporous structure with a similar average pore diameterof around 4.5 nm. On the other hand, the MB molecule has aparallelepiped shape with dimensions 1.7 � 0.76 � 0.325 nm andits attachment on biomass surface may be done with differentorientations [26]. Other workers have reported that the presenceof mesopores (average pore diameter of 2–50 nm) is favorable forMB adsorption by various adsorbents [5,25]. Assuming that the MBmolecule lies flat on the biomass surface even on its largest face(1.7 nm) which is smaller than the reported average pore radius ofA. platensis (2.25 nm), the MB biosorption in this study may also bedue to the intra-particle diffusion of MB molecules in themesopores and due to the entrapment in intrafibrillar capillariesand spaces of the structural exopolysaccharides [6]. This assump-tion agrees with the diffusion analysis of the kineticdata. Therefore, the mesoporous structure of A. platensis canfacilitate the accommodation of MB molecules in the biomasspores [13].

Conclusions

Dry biomass of A. platensis was used as biosorbent formethylene blue removal in batch mode with respect to solutionpH, contact time, initial dye concentration, temperature and ionicstrength. This study applied for the first time a kinetic and

Table 4Amount of cations released from A. platensis biomass (0.5 g/L) after MB biosorption(C0 = 100 mg/L, pH 7.5).

Cations released Temperature (K)

298 308 318

Na+ (mmol/L) Background release 0.512 0.561 0.545After MB biosorption 0.617 0.534 0.564Net release 0.105 �0.027 0.019

K+ (mmol/L) Background release 0.112 0.206 0.171After MB biosorption 0.237 0.169 0.189Net release 0.125 �0.037 0.018

Total net release (mmol/L) 0.230 �0.064 0.037Equilibrium pH 7.53 7.63 7.68qe (mmol MB/g) 0.280 0.257 0.205

0

10

20

30

40

50

60

70

80

90

100

q e (m

g/g)

Co (mg MB/L)

untreat ed

modified

Fig. 9. Biosorption of MB onto untreated and chemically modified biomass of A.platensis at 298 K (C0 = 100 mg MB/L, pH 7.5).

678 D. Mitrogiannis et al. / Journal of Environmental Chemical Engineering 3 (2015) 670–680

thermodynamic analysis for the biosorption of a cationic dye ontoA. platensis. In addition, the role of ion exchange mechanism wasdirectly investigated by detection measures. The kinetic data werefitted very well by the pseudo-second order model, and equilibri-um was achieved within 60–120 min. It was found that the film andintra-particle diffusion contributed to the MB biosorption process.The biosorption capacity of A. platensis for MB increased withincreasing initial dye concentration and decreased with increasingtemperature. At all studied temperatures, the Langmuir, Freundlichand Dubinin–Radushkevich isotherm models fitted well theexperimental equilibrium data, indicating that MB biosorptionwas a complex process, involving more than one mechanism. Thecarboxyl groups of biomass surface contributed to MB chemisorp-tion. The important role of hydrophobic interactions in MB removalwas indicated by the considerable biosorption capacity at low pHvalues and in the presence of NaCl in the sorption solution. Therelease of Na+ and K+ cations from the biomass surface in thesolution after MB sorption confirmed the contribution of cationexchange mechanism. Physical sorption and ion exchange were thedominant mechanisms of MB biosorption at lower temperature.According to the thermodynamic analysis of equilibrium data, MBbiosorption onto A. platensis was a spontaneous, favorable andexothermic process. It was concluded that A. platensis biomass hasa great potential for removal of MB from aqueous solutions.

Acknowledgement

Professor D. Georgakakis of Agricultural University of Athens iskindly acknowledged for his valuable support in respect to theavailability of laboratory equipment.

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