Journal of Colloid and Interface Science 418 (2014) 113–119

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Journal of Colloid and Interface Science

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Removal of the surfactant sodium dodecylbenzenesulfonate from waterby processes based on adsorption/bioadsorption and biodegradation

0021-9797/$ - see front matter � 2013 Elsevier Inc. All rights reserved.http://dx.doi.org/10.1016/j.jcis.2013.12.001

⇑ Corresponding author. Fax: +34 958248526.E-mail addresses: bautista@ugr.es (M.I. Bautista-Toledo), jrivera@ugr.es

(J. Rivera-Utrilla), ppmendez@ugr.es (J.D. Méndez-Díaz), mansanch@ugr.es(M. Sánchez-Polo), fmarin@ugr.es (F. Carrasco-Marín).

María Isidora Bautista-Toledo, José Rivera-Utrilla ⇑, José Diego Méndez-Díaz, Manuel Sánchez-Polo,Francisco Carrasco-MarínDepartment of Inorganic Chemistry, Faculty of Science, University of Granada, 18071 Granada, Spain

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

Article history:Received 30 September 2013Accepted 1 December 2013Available online 8 December 2013

Keywords:SurfactantBacteriaActivated carbonBioadsorptionBiodegradation

This study analyzed the bioadsorption/biodegradation kinetics of the surfactant sodium dodecylbenzene-sulfonate (SDBS) on commercial activated carbons and on activated carbons prepared in the laboratory byactivation of almond shells. The effect of surface oxygen species on these processes was also investigatedby using an activated carbon from almond shells oxidized with H2O2 or HNO3. SDBS removal kinetics fol-lowed a first-order kinetic model, with rate constants between 1.25 � 10�2 h�1 and 2.14 � 10�2 h�1. Theremoval rate constants of total organic carbon (TOC) were also determined, obtaining values rangingbetween 0.51 � 10�2 h�1 and 1.76 � 10�2 h�1. TOC removal rate constants were lower than SDBS removalrate constants, demonstrating that SDBS is also biodegraded during bioadsorption. Both the inorganiccarbon concentration and the colony forming units confirm this biodegradation. The amount of SDBSremoved from water varies between 109.0 and 232.3 mg SDBS/g of carbon. When SDBS adsorption onactivated carbon is conducted in the presence of bacteria, which is the real situation in water treatmentplants, a fraction of bacteria are adsorbed on the surface of activated carbon. A part of the SDBS isremoved by adsorption (bioadsorption) and other part by biodegradation.

� 2013 Elsevier Inc. All rights reserved.

1. Introduction

Surfactant-based processes are becoming increasingly impor-tant in pollution control. The dual hydrophobic/hydrophilic(amphiphilic) nature of surfactant molecules causes them to accu-mulate in interfacial regions, where both the hydrophobic andhydrophilic segments can participate in favorable intermolecularinteractions [1]. Surfactants are widely exploited in industrialprocesses and in consumer product formulations for emulsionstabilization, foaming, detergent action, wetting, mineral separa-tions, pharmaceutical formulation, and other purposes [2].

The presence of surfactants in wastewater poses challengingproblems for subsequent biological or physical–chemical processes[3]. The average surfactant concentration in domestic wastewateris 1–10 mg/L, and the average concentration in wastewateroriginating from the surfactant-manufacturing industries rarelyexceeds 300 mg/L [4]. Sewage treatment plants reduce concentra-tions in raw sewage (1–3 mg/L) but leave sufficiently high concen-trations in the sludge to represent a potential environmentalproblem [5–7].

Surfactants can be removed from urban and industrial waste-waters by adsorption on activated carbons [8] or by biologicaldegradation with activated sludge [9]. Although numerous studieshave demonstrated that most commercial surfactants are degradedin an aerobic medium at low concentrations, this biodegradabilitymay be hindered in anaerobic media or when the surfactants arepresent at elevated concentrations, e.g., in effluent from industrialprocesses and other technologies using surfactants for recoverypurposes.

The biodegradation under aerobic conditions of linear alkylben-zenesulfonates (LAS), one of the most widely utilized families ofanionic surfactants, has been the object of numerous studies; thesehave yielded considerable evidence on the first biotransformationcycle (primary biodegradation), beginning with the oxidation ofexternal methyl groups [2], giving rise to the formation of sulf-ophenyl carboxylic acids (SPACs). Finally, benzene ring openingand/or desulfonation takes place in the last biodegradation or min-eralization phase, generating CO2, H2O, inorganic salts, and bio-mass. Nielsen et al. [10] confirmed that the microbial populationof domestic and industrial activated sludge is highly effective inthe primary biodegradation of LAS but is not capable of mineraliz-ing most of the related metabolites.

A previous study [11] found that the presence of bacteria duringthe adsorption of sodium dodecylbenzenesulfonate (SDBS), awidely used anionic surfactant from the LAS family, accelerates

114 M.I. Bautista-Toledo et al. / Journal of Colloid and Interface Science 418 (2014) 113–119

and increases its adsorption on activated carbon. The adsorption ofmicroorganisms on the activated carbon surface increases itshydrophobicity, explaining the results obtained. Moreover, underthe same experimental conditions, bacteria from the biologicaltreatment of a wastewater treatment plant were not able to de-grade SDBS.

With this background, the objective of this study was to furtherstudy the removal of SDBS from water by the combined use of acti-vated carbon and previously adapted bacteria to enhance SDBSbiodegradation and bioadsorption. In this study both commercialactivated carbons and activated carbons prepared in the laboratoryby physical activation of almond shells will be used. The effect ofsurface oxygen species on these SDBS removal processes was alsoinvestigated by using an activated carbon from almond shellsoxidized with H2O2 or HNO3.

2. Materials and methods

2.1. Activated carbons

Eight activated carbons were selected for this study: three com-mercial carbons, Norit (Sorbonorit), Merck, and Ceca (AC40) (S, M,and C, respectively); and five carbons prepared in our laboratory,three of which obtained by carbonizing almond shells in N2 flowat 1273 K for 1 h and then activating them with water vapor at1123 K for 2.5, 5, and 8 h (samples A-2.5, A-5, and A-8, respec-tively), with a percentage burn-off of 25.0%, 42.0%, and 61.4%,respectively. The other two activated carbons were obtained byintroducing oxygen groups onto the carbon A-8 surface by usingtwo different oxidation processes: (i) treatment with HNO3 14 Mat 353 K until dryness and subsequent washing with distilledwater until nitrate removal (determined with brucine), and (ii)treatment with H2O2 (9.8 M) at 298 K under constant agitationfor 48 h. These activated carbon samples are referred to hereafteras A-8N and A-8O, respectively.

All activated carbon samples were characterized by N2 adsorp-tion at 77 K. The BET equation was applied to the nitrogen adsorp-tion isotherms to obtain their surface area (SN2). Mercuryporosimetry was carried out at 4200 kg cm�1 (QuantachromeAutoscan 60, porosimeter), yielding the volumes of pores with adiameter of 3.7–50 nm, V2, and with a diameter >50 nm, V3. Wealso determined the pH of the point of zero charge, pHpzc, andthe ash and oxygen contents by using previously publishedmethods [12].

2.2. Sodium dodecylbenzenesulfonate and its determination

SDBS of reagent quality was acquired from Aldrich and spectro-photometrically determined in aqueous solution at 223 nm wave-length in a SPECTRONIC GENESIS 5 apparatus. High performanceliquid chromatography (HPLC) in gradient elution mode was usedto follow the SDBS degradation in the presence of the reactionbyproducts generated by its biodegradation [13].

2.3. Microorganisms

The bacteria used in this study were obtained from the water ofa treatment plant that uses activated sludge. This water wasenriched with bacteria capable of degrading SDBS by adding5 mL in an Erlenmeyer flask with 25 mL Tryptic Soy Broth (TSB)solution and buffer at pH 7, sterilizing in autoclave, and agitatingat a temperature of 303 K until turbidity was observed in the solu-tion. Then, 100 mg SDBS was added to the solution in order toadapt the microorganisms to the surfactant for its degradation. Asubculture was obtained by transferring 2 mL of the previous

culture into 25 mL of sterile TSB and mixing it with 100 mg SDBS,repeating this process several times. Finally, bacteria weregathered by centrifugation and washed with sterilized water inautoclave to obtain a bacteria-rich suspension capable of degradingSDBS.

The number of colony forming units (CFUs) was determined bydrawing 50-lL volumes of an SDBS solution, 250 mg L�1, withbacteria and activated carbon and diluting with 4.95 mL sterile dis-tilled water. The suspensions were then serially diluted for bacteriacounts in plates with culture medium containing Agar (TryptoneSoy Agar) (TSA) at different periods of time.

2.4. Experimental methods

SDBS adsorption kinetics on activated carbons and the kineticsof its aerobic biodegradation were obtained by placing 100 mL ofa saline medium solution (K2HPO4, 3.5 g L�1; KH2PO4, 1.5 g L�1;NH4Cl, 0.15 g L�1; NaCl, 0.5 g L�1; Na2SO4, 0.15 g L�1) in flasks con-taining 250 mg L�1 SDBS and 0.1 g activated carbon; 1 mL of theabove-reported bacteria solution was added to these solutions.Flasks were maintained under constant agitation at 298 K, and sam-ples were drawn after different contact times to determine the SDBSand total organic carbon (TOC) concentrations in the solution. In par-allel, two experiments identical to the above were performed exceptthat one was in the absence of activated carbon, enabling the analy-sis of SDBS and TOC removal due to biodegradation alone, and theother was in the absence of bacteria, revealing the amount of SDBSremoved by activated carbon adsorption alone. The solution pHwas 7 in all adsorption/bioadsorption experiments.

In order to analyze the biodegradation at low SDBS concentra-tions, 100 mL SDBS solutions at 10 mg L�1 and 20 mg L�1 wereplaced in contact with 1 mL of the above-reported bacterialsuspension, and another experiment was performed using amixture of 20 mg L�1 SDBS solution with the bacteria suspensionand activated carbon S. The SDBS concentration was determinedat different time points.

The total organic and inorganic carbon values in the solutionwere measured by using a Shimadzu TOC-5000A unit. SDBS solu-tion toxicity was determined with Dr. Lange LUMIStox 300 equip-ment comprising a bioluminescence-measuring instrument andincubation unit, according to the UNE-EN ISO 11348-2 guideline[14]. This determination is based on the inhibition of luminousintensity of the marine bacteria Vibrio fischeri, NRRL-B-11177, after15 min of exposure to the sample. In all measurements, the per-centage inhibition (%I) was obtained by comparing the responseof a control saline solution with that of the sample. Toxicity wasexpressed as the percentage inhibition of bacterial growth as afunction of treatment time.

3. Results and discussion

3.1. Characterization of activated carbon samples

Table 1 lists the characteristics of the activated carbons used inthis study. The commercial carbons have a high ash content (>5%)increasing in the order M < S < C, whereas the ash contents of thealmond shell-derived carbons are very low (<0.1%). The surfaceareas of the commercial carbons are >1200 m2 g�1. We highlightthe large surface area (1600 m2 g�1) of the carbon obtained byactivating almond shells for 8 h, with a lower surface area beingobserved after shorter almond shell activation times, decreasingto a value of 825 m2 g�1 after activation for 2.5 h. Sample A-8 alsohas the largest external surface area.

Carbon C is slightly acidic, carbon M is neutral, and carbon S isbasic (Table 1). The original almond shell-derived carbons are

Table 1Chemical and textural characterization of activated carbon samples.

Carbon SN2 (m2 g�1) Sext (m2 g1) V2 (cm3 g�1) V3 (cm3 g�1) Ash (%) pHPZC Oxygen wt (%)

C 1201 21.3 0.046 0.409 8.12 6.0 10.1M 1301 41.9 0.101 0.284 5.30 7.7 7.4S 1182 39.4 0.085 0.481 6.07 9.0 9.5A-2.5 825 22.5 0.078 0.078 0.05 10.4 0.6A-5 1290 38.2 0.119 0.155 0.08 10.6 0.4A-8 1600 65.9 0.225 0.309 0.10 11.1 0.4A-8O 1400 59.1 0.200 0.243 n.d. 4.7 4.4A-8N 820 34.8 0.114 0.194 n.d. 2.3 20.4

SBET = Apparent surface area determined by applying BET equation to N2 adsorption isotherm.Sext = External surface area determined by mercury porosimetry.V2 = Volume of pores with diameter of 50–3.7 nm, determined by mercury porosimetry.V3 = Volume of pores with diameter above 50 nm, determined by mercury porosimetry.n.d. = not determined.

0.0

0.5

1.0

0 125 250t (h)

SDB

S/SD

BS

0

a

0.0

0.5

1.0

0 125 250t (h)

SDB

S/SD

BS

0

b

Fig. 1. SDBS removal by the different activated carbons in the presence of bacteriaas a function of time. (a) (�), S; (N), M; (d), C; and (b) (4), A-8; (h), A-5; (j), A-2.5;(s), A-8N; (}), A-8O; ( ), Bacteria without carbon. pH = 7, [SDBS]0 = 250 mg L�1,T = 298 K, [Activated carbon] = 1 g/L.

M.I. Bautista-Toledo et al. / Journal of Colloid and Interface Science 418 (2014) 113–119 115

basic, with pHPZC values between 10.4 (carbon A-2.5) and 11.1(carbon A-8). However, the treated almond shell-derived carbonsare acidic, with pHPZC values lower than 5. The oxygen content ofcommercial carbons increases in the order M < S < C, whereas itis very low in the almond shell-derived carbons (0.4–0.6%). Thetreated almond shell-derived carbons increased their oxygen con-tent up to 4.4 (sample A-8O) and 20.4 (sample A-8N).

The surface area and pore volume of carbon A-8 are reducedafter oxidization with nitric acid or hydrogen peroxide and arelowest after nitric acid treatment, which may be attributable tothe oxidation and destruction of the pore walls in addition toobstruction by oxygenated groups formed at the pore entrance[15]. This effect was more marked in the HNO3� than in theH2O2-treated samples because the extent of the carbon oxidationis greater, as demonstrated by the higher increase in oxygencontent in the former (Table 1). A previous study [15], using theFourier-transform infrared spectroscopy technique, found thatHNO3 treatment (sample A-8N) fixes carboxylic acid groups alongwith nitro and nitrate groups, whereas H2O2 treatment (sampleA-8O) fixes carboxylic and lactone groups.

Programmed thermal decomposition of these samples was usedto determine the amounts of CO and CO2 generated in the decom-position of surface oxygen groups (Table 1-SM), and both weremuch larger in sample A-8N, due to the higher number of oxygen-ated groups created by the HNO3 treatment. As previously reported[15–17], the CO2 is generated by thermal decomposition of carbox-ylic, anhydride (acid), and lactone groups, whereas the CO derivesfrom phenol, carbonyl, quinone, pyrone, and anhydride (acid)groups. We highlight that the values of the CO/CO2 relationshipare nearly threefold higher in A-8O (5.3) than in A-8N (1.9)(Table 1-SM), which may be related to the higher proportion of car-boxylic groups in sample A-8N and of phenol groups in sampleA-8O.

The surface hydrophobicity of activated carbons is closely re-lated to their surface oxygen groups [18,19]. A reduction in theoxygen content of activated carbons increases their hydrophobicityand therefore favors organic compound adsorption. Hydrophobic-ity also affects bacterial surface adhesion [20–22].

3.2. SDBS bioadsorption

Fig. 1a depicts the SDBS bioadsorption/biodegradation kineticson the commercial activated carbons and the biodegradation kinet-ics in the absence of activated carbon. Fig. 1b shows the SDBS bio-adsorption/biodegradation kinetics on the almond-shell carbons.First- and second-order kinetic models were applied to the bioad-sorption kinetics.

The first-order kinetic model, also known as the Lagergren mod-el, has been extensively used to interpret the adsorption rate of

organic compounds on different adsorbents [23,24] and can berepresented by the following equation:

dqdt¼ k1ðqe � qÞ ð1Þ

where q is the adsorbed amount as a function of time, qe is theamount adsorbed at equilibrium, and k1 is the removal rate con-stant. This equation can be integrated by using the initial conditionq = 0 when t = 0, obtaining:

q ¼ qe 1� ek1 t� �

ð2Þ

0.0

1.0

2.0

3.0

SBET (m 2×g-1)

k 1×1

02(h

-1)

0.0

1.0

2.0

3.0

400 800 1200 1600

Fig. 2. Relationship between SDBS removal first order kinetic constant and theactivated carbon surface area. pH = 7, [SDBS]0 = 250 mg L�1, T = 298 K, [Activatedcarbon] = 1 g/L.

116 M.I. Bautista-Toledo et al. / Journal of Colloid and Interface Science 418 (2014) 113–119

Expression of this equation in terms of adsorbate concentra-tions CA and CA0 results in:

CA ¼ CA0 �mV

� �qe 1� e�k1t� �

ð3Þ

The second-order kinetic model can be represented by the fol-lowing differential equation [25].

dqdt¼ k2 qe � qð Þ2 ð4Þ

Integrating equation and using the initial condition q = 0 whent = 0, the following equation is obtained:

q ¼ q2e k2t

1þ qek2tð5Þ

This equation can also be expressed in terms of CA and CA0:

CA ¼ CA0 �mV

� � q2e k2t

1þ qek2tð6Þ

Table 2 exhibits the kinetic parameters obtained by applyingboth models to the data in Fig. 1a and b. The kinetic curves per-fectly fit first-order kinetics, as demonstrated by the values ofthe regression coefficient, R2, close to unity, and by the similaritybetween the values of experimental qe, qe(exp), and model-calcu-lated qe, qe(calc). Among the commercial carbons, carbon M showsthe highest SDBS adsorption rate constant (1.60 � 10�2 h�1),although it is lower than that of carbon A-8 (2.14 � 10�2 h�1).When the values of these constants are related to the chemicaland textural characteristics of the activated carbons, it can be ob-served that, in general, the SDBS removal rate constant rises withlarger carbon surface area (Fig. 2) and decreases with lower carbonoxygen content (Tables 1 and 2). The surface area of a carbonenhances adsorption/bioadsorption processes by increasing thesolid–liquid interface and hence the effectiveness of the process.The presence of oxygen on the carbon surface reduces the bioad-sorption by decreasing its hydrophobicity and consequentlyincreasing the competition of water with adsorbates for the carbonadsorption sites [26].

The percentage removal of SDBS was determined after contactwith the carbon and/or bacteria for 10 days (Table 2-SM). The SDBSbiodegradation by bacteria was very low (16%) in the absence ofactivated carbon and considerable increased in its presence dueto the bioadsorption of SDBS on the activated carbon. The orderof percentage removal is the same as the order of rate constants(Table 2), with carbon A-8 having the highest SDBS bioadsorptioncapacity, attributable to its larger surface area and lower oxygencontent.

The importance of carbon surface oxygen groups in SDBS bioad-sorption is demonstrated by comparing the results obtainedamong samples A-8, A-8O, and A-8N. Tables 2 and 2-SM show adrastic reduction in the bioadsorption capacity of carbon A-8 afterHNO3 treatment (sample A-8N), with a lesser reduction after H2O2

Table 2Parameters of SDBS removal kinetics in the presence of carbon and bacteria.

Carbon qe (exp) (mg/g) First order model

k1�102 (h�1) R2 qe (ca

C 212.8 1.39 0.996 220.1M 224.3 1.60 0.997 254.6S 218.7 1.27 0.981 211.4A-2.5 130.2 1.28 0.940 120.0A-5 206.6 1.46 0.997 207.1A-8 232.3 2.14 0.998 242.2A-8O 214.0 1.48 0.991 212.9A-8N 109.5 1.25 0.998 117.7

treatment (sample A-8O). This decrease in bioadsorption capacityis related to the reduction in carbon surface area after treatmentwith oxidizing agents and to the increase in oxygenated groupson the carbon surface. These surface groups reduce the carbonhydrophobicity and therefore its capacity to adsorb bacteria, whichare hydrophobic through the presence of phospholipids on theircell walls [27,28].

A further negative effect of the carbon surface oxygenatedgroups on SDBS adsorption is that those which are electronic deac-tivators, such as the carboxylic groups, mainly present on the A-8Nsample, weaken dispersive interactions (p–p type) between theelectrons of the SDBS aromatic ring and the graphene planes ofthe carbon, which are deactivated by the presence of these groups[29]; this partly reduces the performance of the adsorption processand explains the low adsorption capacity of the A-8N sample. Incontrast, the presence of phenol groups (electronic activators) onthe A-8O sample increases the electronic density of the grapheneplanes of the activated carbon and therefore the p–p adsorbate–adsorbent interactions, enhancing its adsorption capacity.

Regarding SDBS-activated carbon electrostatic interactions, wehighlight that SDBS (pKa = 3.08) appears as anion at the study pH(pH = 7), and the sign of the carbon surface charge depends on itspHpzc value (Table 1). Thus, the charge is positive on samples S,A-2.5, A-5, and A-8 but negative on samples A-8O and A-8N. Thesurface charge density of samples C and M is close to zero. Hence,electrostatic interactions of SDBS with carbons S, A-2.5, A-5, andA-8 are attractive, favoring the adsorption process, and those withcarbons A-8O and A-8N are repulsive. This in part explains the lowadsorption capacity of these two samples.

Second order model

lc) (mg/g) k2�105 (L�(mg h)�1) R2 qe (calc) (mg/g)

3.10 0.966 342.35.28 0.958 291.63.59 0.950 301.45.92 0.872 169.54.07 0.983 288.16.51 0.987 294.15.60 0.951 271.16.75 0.982 150.1

0.0

0.5

1.0

t (h)

TOC

/TO

C0

a

0.5

1.0

0 125 250

C/T

OC

0

M.I. Bautista-Toledo et al. / Journal of Colloid and Interface Science 418 (2014) 113–119 117

Previous studies by our research group [30] demonstrated thatbacteria are adsorbed on the porous surface of the activated car-bon, which would a priori favor SDBS removal for the following.On the one hand, the bacteria transform the biodegradable portionof SDBS into biomass and CO2 before it occupies adsorption sites onthe carbon surface. On the other hand, bacteria adsorption in-creases the carbon surface hydrophobicity from the presence ofphospholipids on the cells, thereby enhancing SDBS adsorptionthrough their hydrophobic aliphatic chain [31]. Fig. 3 depicts, asan example, the scanning electron microscopy images of carbon Sbefore (a) and after (b) contact with bacteria. It can be observedthat when the carbon has been in contact with bacteria, some ofthem are retained on its surface.

Fig. 4a and b depict the time course of the solution TOC duringSDBS bioadsorption/biodegradation on the commercial and al-mond-shell activated carbon samples, respectively. The kineticcurves of TOC reduction, like those obtained for SDBS removal fitfirst-order kinetics, while the rate constants, k1, (Table 3) obtainedfor TOC reduction are lower than those obtained for SDBS removal.The reduction in the k1 value for TOC removal (Table 3) with re-spect to the k1 value for SDBS removal (Table 2) ranges between12% (Carbon S) and 59% (Carbon A-8N). These results indicate thatTOC removal is slower than SDBS removal in all cases, demonstrat-ing the biodegradation of part of the SDBS, which producesbyproducts that are subsequently adsorbed by the carbons.

Fig. 3. Scanning electron microscopy images of carbon S in the absence (a) andpresence (b) of bacteria.

0.0

0 125 250

t (h)

b

TO

Fig. 4. TOC removal by the different activated carbons in the presence of bacteria asa function of time. (a) (�), S; (N), M; (d), C; and (b) (4), A-8; (h), A-5; (j), A-2.5;(s), A-8N; (}), A-8O; ( ), Bacteria without carbon. pH = 7, [SDBS]0 = 250 mg L�1,T = 298 K, [Activated carbon] = 1 g/L.

Fig. 1-SM in Supplementary Material depicts, as an example, thetime course of inorganic carbon (IC) present in the solution duringSDBS bioadsorption/biodegradation when using carbons M, C, andA-8, also showing the results obtained in the absence of carbon.During these processes, there is an increase in IC versus baseline(close to 1 mg L�1) of up to threefold the original amount; this in-crease is attributable to the increased CO2 produced by the bacte-rial degradation of SDBS [32,33]. Hence, all of these resultsdemonstrate a biodegradation of the surfactant alongside itsbioadsorption.

The effect of the presence of bacteria in water on SDBS adsorp-tion was analyzed by studying this process in the absence of bac-teria. Table 2-SM and Table 4 exhibit the results obtained,showing that, in general, the adsorption rates and percentage SDBSremoved are highly similar to those obtained in the presence ofbacteria (Table 2 and 2-SM). These results indicate that theabove-reported beneficial effects of the bacteria on SDBS bioad-sorption are counteracted by the blockage of activated carbonporosity produced by bacteria adsorption [30], reducing the effec-tive carbon surface for SDBS adsorption.

3.3. SDBS biodegradation

The effect of biodegradation on SDBS removal was assessed byseparating the products present in the solution by HPLC at theend of the bioadsorption/biodegradation experiments, i.e., after10 days of contact. Fig. 2-SM in Supplementary Material depicts,

Table 3Parameters of TOC removal kinetics in the presence of carbon and bacteria.

Carbon qe (exp) (mg/g) First order model Second order model

k1�102 (h�1) R2 qe (calc) (mg/g) k2�105 (L�(mg h)�1) R2 qe (calc) (mg/g)

C 158.6 1.04 0.997 143.0 12.80 0.961 166.9M 159.9 1.31 0.978 206.3 9.82 0.981 190.6S 144.4 1.13 0.976 116.9 3.15 0.918 224.3A-2.5 146.2 0.55 0.905 122.6 25.1 0.951 110.9A-5 157.5 1.00 0.967 130.7 3.18 0.962 314.5A-8 160.6 1.76 0.988 146.5 15.1 0.998 185.2A-8O 158.2 1.33 0.952 152.5 7.59 0.936 197.5A-8N 146.1 0.51 0.843 118.7 31.6 0.943 105.0

Table 4Parameters of SDBS removal kinetics in the presence of activated carbon and absence of bacteria.

Carbon qe (exp) (mg/g) First order model Second order model

k1�102 (h�1) R2 qe (calc) (mg/g) k2�105 (L�(mg h)�1) R2 qe (calc) (mg/g)

C 220.8 1.63 0.993 248.07 12.90 0.969 277.3M 226.8 1.83 0.994 206.34 5.28 0.980 291.6S 210.0 1.25 0.966 254.70 0.81 0.700 457.1A-2.5 112.5 1.27 0.968 120.04 7.54 0.978 170.1A-5 204.9 1.46 0.997 196.18 4.07 0.990 288.1A-8 229.8 1.74 0.997 213.01 6.51 0.999 294.1A-8O 211.0 1.48 0.994 212.93 5.60 0.987 271.1A-8N 97.8 1.25 0.978 97.16 8.22 0.909 134.4

10

20

30

40

50

0 20 40 60Carbon S + Bacteria

Carbon S0

10

20

30

40

50

Inhi

bitio

n (%

)

t (h)

Fig. 5. Time course of toxicity during SDBS removal by activated carbon S in boththe absence and presence of bacteria. pH = 7, [SDBS]0 = 250 mg L�1, T = 298 K,[Activated carbon] = 1 g/L.

0.0

0.5

1.0

0.0 0.5 1.0

C/C 0

TOC

/TO

C0

Fig. 6. Relationship between TOC and SDBS removal by the activated carbon/bacteria systems. pH = 7, [SDBS]0 = 250 mg L�1, T = 298 K, [Activated carbon] = 1 g/L. (N), M; (4), A-8; (s), A-8N; (}), A-8O.

118 M.I. Bautista-Toledo et al. / Journal of Colloid and Interface Science 418 (2014) 113–119

as an example, the results obtained after the contact of SDBS withcarbon S (a), carbon S with bacteria (b), and bacteria alone (c).Chromatograms (b and c) shows, along with the characteristicSDBS peak at three minutes, other peaks that are not observed inthe chromatogram (a). These results again confirm that SDBS ispartly biodegraded during its bioadsorption, given that the newpeaks in the chromatograms of solutions with bacteria correspondto SDBS biodegradation products (SPACs) [2,34,35], which aremore hydrophilic than SDBS and therefore elute more rapidly. Itis important to note that, according to the magnitude of the chro-matogram peaks in Fig. 2-SM in Supplementary Material, the ex-tent of SDBS biodegradation is greater in the presence of theactivated carbon, indicating that the adhesion of bacteria on thecarbon favors the metabolism and growth of the bacteria.

In order to determine possible bacterial growth during SDBSbioadsorption/biodegradation in the presence of activated carbon,the variation in the number of CFUs was calculated as a functionof the contact time, quantifying the CFUs at baseline and atdifferent treatment times. The initial amount of bacteria placedin contact with the carbon and SDBS was 2.25 � 106 CFU/mL.Fig. 3-SM in Supplementary Material depicts, as an example, the

CFU values throughout SDBS bioadsorption/biodegradation onactivated carbon S. An increase in CFUs can be observed duringthe first 115 h of treatment, rising from 2.25 � 106 CUF/mL at base-line to 4.5 � 106 CUF/mL; a progressive decrease in CFUs is seenfrom 115 h of contact onwards. This behavior, which is natural ina bacteria culture cycle, again demonstrates SDBS biodegradation,which permits the proliferation of these microorganisms.

Fig. 4-SM in Supplementary Material shows the SDBS removalresults during biodegradation experiments at low SDBS concentra-tions in the absence and presence of activated carbon S. Comparisonof these results with those in Fig. 1 shows that low SDBS concentra-tions yield a higher percentage biodegradation, although theactivated carbon–bacteria system, which produces both bioadsorp-tion and biodegradation, remains more effective for SDBS removal.

The solution toxicity is an important issue for the technicalapplicability of these processes. Fig. 5 depicts the system toxicity

M.I. Bautista-Toledo et al. / Journal of Colloid and Interface Science 418 (2014) 113–119 119

during SDBS bioadsorption/biodegradation with carbon S in com-parison to the toxicity during SDBS adsorption on carbon S in theabsence of bacteria. The toxicity (percentage inhibition) decreasesfrom 47% to 23% in the presence of bacteria but to only 40% in theirabsence. This greater toxicity reduction in the presence of bacteriamust be related to the metabolism of the bacteria and the decreasein toxicity of the SDBS biodegradation compounds produced whenbacteria are present in the system.

Finally, Fig. 6 depicts, as an example, the relationship betweenthe time courses of TOC and SDBS concentrations in the solutionduring bioadsorption/biodegradation with carbons M, A-8, A-8O,and A-8N. In all cases, the points are below the bisector of the plotat baseline, indicating the slower adsorption of SDBS biodegrada-tion byproducts than of SDBS itself; however, with longer treat-ment time, these byproducts are adsorbed on the commercialand almond shell-derived carbons. However, on oxidized carbons,mainly those oxidized with HNO3, complete adsorption of thesebyproducts is not attained. This behavior is due to the highlyhydrophilic nature of SDBS biodegradation byproducts and of acti-vated carbons. This hydrophobicity is enhanced on carbon A-8N,which presents a 20.4% oxygen content.

4. Conclusions

The bioadsorption/biodegradation kinetics of the surfactantSDBS was investigated on commercial activated carbons and onthose prepared by chemical activation of almond shells. The effectsof the textural and chemical characteristics of activated carbons onthese kinetic processes were also analyzed. SDBS bioadsorption onactivated carbon was previously studied [11], and it was found thatthe presence of microorganisms enhanced the SDBS adsorptioncapacity of activated carbons because adsorption of the bacteriaincreased the hydrophobicity of the carbon surface. It was also re-ported [36] that LAS biodegradation is enhanced in the presence ofa solid support such as glass beads, due to the formation on theglass support of a biofilm that is continuously exposed to the sur-factant, with a longer contact time in comparison to suspendedbacteria [37]. Both processes (SDBS biodegratation and bioadsorp-tion on activated carbon) were investigated together for the firsttime in the present study, which showed that they take placesimultaneously. This study demonstrates that when SDBS adsorp-tion is conducted in the presence of bacteria, i.e. the real-life situ-ation in water treatment plants, a fraction of the bacteria areadsorbed on the surface of activated carbon, favoring the removalof one part of the SDBS by adsorption (bioadsorption) and the otherpart by biodegradation.

SDBS removal rate constants and the amounts removed in equi-librium largely depend on the surface area and oxygen content ofthe carbon. Moreover, during SDBS removal, the system toxicity isreduced by the bioadsorption of both SDBS and its biodegradationbyproducts on activated carbons, mainly on untreated carbons.

For all activated carbons studied, the TOC removal rate con-stants are lower than the SDBS removal rate constants, confirmingthat SDBS biodegradation also takes place during bioadsorption.Moreover, for the oxidized activated carbons, especially the sampleoxidized with nitric acid, the percentage TOC removed in equilib-rium is lower than the percentage SDBS removed in equilibrium,indicating that SDBS biodegradation compounds, which are morehydrophobic than SDBS, are not completely adsorbed on thesecarbons.

Taken together, these results suggest that bioadsorption andbiodegradation may occur in many natural processes in parallel

with physical or chemical adsorption. This may explain discrepan-cies between theoretical studies and experimental data when onlyphysical or chemical adsorption is taken into account.

Acknowledgments

The authors are grateful for the financial support provided byMEC-DGI and FEDER (CTQ2011-29035-C02-02), and the Junta deAndalucía (RNM7522).

Appendix A. Supplementary material

Supplementary data associated with this article can be found, inthe online version, at http://dx.doi.org/10.1016/j.jcis.2013.12.001.

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