Arthrospira ( Spirulina ) Species as Bioadsorbents for Lead, Chromium, and Cadmium - a Comparative Study

Sundaramoorthy BalajiThiagarajan Kalaivani*Chandrasekaran RajasekaranMohan ShaliniRamamoorthy SivaRajan Kumar SinghMohammed Asif Akthar

School of BioSciences andTechnology, VIT University, Vellore,Tamil Nadu, India

Research Article

Arthrospira (Spirulina) Species as Bioadsorbentsfor Lead, Chromium, and Cadmium – aComparative Study

Arthrospira (Spirulina) belongs to the cyanobacterial family has been reported as apotential bioremediation agent. The bioadsorption potential of Arthrospira species,namely A. indica, A. maxima, and A. platensis, was tested against lead, chromium, andcadmium toxicity under laboratory conditions. Arthrospira species were cultured inZarrouk’s medium containing lead, chromium, and cadmium with two varyingconcentrations (0.01 and 0.05mM) and in river water contaminated with tanneryeffluent containing these heavy metals. Parameters like specific growth rate, totalchlorophyll, and total protein contents were analyzed and compared. Specific growthrate, total chlorophyll, and total protein contents possess dose dependent decrease withincrease in concentrations of metals and also in heavy metal contaminated tanneryeffluent when compared with control. Statistical analysis revealed that there is a goodcorrelation between the specific growth rate and protein content in all the species.Atomic absorption spectrometry analysis also revealed that there is a maximumbioadsorption potential of the Arthrospira species. Results indicated that the threeArthrospira species used in this experiment were found to be potential candidates forbioadsorption against lead, chromium, and cadmium.

Keywords: Bioadsorption; Cyanobacteria; Heavy metals; Tannery effluent; Wastewater treatment

Received: June 18, 2013; revised: January 23, 2014; accepted: February 3, 2014

DOI: 10.1002/clen.201300478

1 Introduction

Worldwide environmental pollution is a threat to the ecosystem dueto the release of toxic heavy metals [1, 2]. Heavy metals like lead,chromium, and cadmium have a wide variety of importantindustrial applications, such as manufacturing storage batteries,printing pigments, fuels, photographic materials, tanning ofleathers, and explosives [3, 4]. From these industries, there is aconsiderable discharge of residual water contaminated with lead,chromium, and cadmium. Lead, chromium, and cadmium are non-biodegradable, causes serious problems to the environment andpublic health when they contaminate the ground water [5, 6]. Heavymetals cause respiratory problems like asthma, adverse effects likebehavioral problems, and learning disabilities in children [7]. InIndia, particularly Vellore District from Tamil Nadu state is facingthe heavy metal pollution problems, because this district is wellknown for tanneries and its associated industries [8]. To overcomethis, the removal of heavy metals like lead, chromium, andcadmium is important for environmental protection and humanhealth. Biological approaches, especially the use of bioadsorbents,

have been evaluated as an alternative to the conventional treatmenttechniques [9–11]. In this context, microalgae like Arthrospira(Spirulina) belong to the cyanobacterial family and are usable asbioadsorbents by virtue of their low cost and relatively high bindingaffinity [12, 13].Arthrospira is a multicellular, filamentous, non-heterocyst cyano-

bacterium reported for its adaptability and bioremedial capabilityagainst heavy metals [14, 15]. The Arthrospira cell wall is made up ofaminic, carboxylic, thiolic, sulfhydrylic, and phosphoric functionalgroups which can bind metal ions on its surface [16–18]. Microalgaelike Arthrospira have been found to be very effective bioadsorbents inremoving heavy metals from wastewater because of their largesurface area and high binding affinity [6, 12]. In order to determinethe feasibility of Arthrospira as a bioadsorbent, the present studycompares the effects of three Arthrospira species namely A. indica,A. maxima, and A. platensis against two different concentrations ofheavy metals viz. lead, chromium, and cadmium metal ions (0.01and 0.05mM) and also river water contaminated with tanneryeffluent. The parameters namely specific growth rate, totalchlorophyll, protein content, and heavy metal analysis using atomicabsorption spectrometry were employed to check the bioadsorptionpotentials of these species.Correspondence: Dr. C. Rajasekaran, Plant Biotechnology Division,

School of Biosciences and Technology, VIT University, Vellore - 632 014,Tamil Nadu, IndiaE-mail: [email protected]

Abbreviations: SGR, specific growth rate; TCC, total chlorophyll content;TPC, total protein content *The author contributed equally to this paper.

1

© 2014 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.clean-journal.com Clean – Soil, Air, Water 2014, 42 (9999), 1–8

2 Materials and methods

2.1 Species and culture conditions

The Arthrospira (Spirulina) species namely A. indica, A. maxima, andA. platensis were obtained from the Centre for Advanced Studies inBotany, University of Madras, Tamil Nadu, India, and preservedin the laboratory for the study. These species were cultured inZarrouk’s liquid medium [19] adjusted to pH 9.5 at 25� 1°C underaseptic conditions. The cultures were gently stirred and illuminatedwith white light produced by neon tubes at 50mmol photonm� 2 s� 1

with a light/dark cycle of 14:10h.

2.2 Collection of effluent

River water contaminated with tannery effluent was collected fromthe estuary of Palar River in Vaniyambadi of Vellore District, TamilNadu, India.

2.3 Treatments

The Arthrospira species A. indica, A. maxima, and A. platensis werecultured in Zarrouk’s medium [20] supplemented with twoconcentrations (0.01 and 0.05mM) [21] of lead, chromium, andcadmium ions. Arthrospira species were also cultured in river watercontaminated with tannery effluent containing heavy metals. Thecontrol organism was grown in Zarrouk’s medium without heavymetal.

2.4 Growth of Arthrospira species

Growth of the Arthrospira species wasmonitored turbidimetrically at560nm [22] and doubling time, specific growth rate were calculated.The formula used for the calculation of doubling time was:

2:303�logðday2Þ

-logðday1Þ�=ðday2-day1Þ

It is expressed in td. The formula used for calculating the specificgrowth rate was:

0:693=td

=mThe species attained the stationary phase after eleven days in both

control and treated samples. Therefore, the specific growth rate,total chlorophyll (TCC), and total protein contents (TPC) weremeasured up to 11 days with different day intervals.

2.5 Chlorophyll estimation

TCC was determined according to the method of Parson andStrickland [23]. Total chlorophyll extraction was done withmethanol by homogenization.

2.6 Protein estimation

Protein estimation was performed by Lowry’s method withmodifications [24]. Samples were taken in different day intervalsand the amount of protein present in the samples was expressed inmg/mL.

2.7 Heavy metal adsorption analyzed by atomicabsorption spectrometry

The Arthrospira cell suspension was analyzed for lead, chromium,and cadmium by atomic absorption spectrometry (Varian 250model) by APHA standard methods [25].

2.8 Statistical analysis

Data were analyzed statistically using the statistical package forsocial sciences version 16.0. Experiments were carried out intriplicate (n¼ 3). The results were reported as mean� SE.

3 Results and discussion

3.1 Effect of lead, chromium, and cadmium toxicityon growth of Arthrospira

In order to investigate the bioadsorption capacity of Arthrospiraspecies and their ability of tolerance was measured in terms ofgrowth rate against lead, chromium, and cadmium. Arthrospiraspecies were cultured in medium containing lead, chromium, andcadmium ions at 0.01 and 0.05mM concentrations, respectively, andthe specific growth rate was measured (Figs. 1–3). According to theFood and Agricultural Organization guidelines, the toxic levels oflead, chromium, and cadmium are 500, 100, and 10mg L� 1,respectively [26, 27]. On this basis, the concentrations of lead,chromium and cadmium were selected for this study. The resultsindicate that the growth rate of all Arthrospira species was maximalin the control compared to the treated samples and a dosedependent decrease in the growth rate against an increase in heavymetal concentration could be seen. At a lower concentration(0.01mM) of these metals, the growth inhibition of Arthrospiraspecies was less.In contrast, at a higher concentration (0.05mM), the growth

inhibition of Arthrospira species was higher and thereby a furtherdecrease in cell growth was observed. When compared with controlthe specific growth rate of A. indicawas found to be 91.66, 98.33, and99.95% for 0.01mM concentration of lead, chromium, and cadmi-um, respectively. The specific growth rate for A. indica was 41.66,54.21, and 57.64% for 0.05mM concentration of lead, chromium, andcadmium, respectively. The specific growth rate for A. maxima was96.15, 89.20, and 95.23% for 0.01mM concentration of lead,chromium, and cadmium, respectively. The specific growth ratefor A. maxima was 46.15, 41.89, and 44.89% for 0.05mM concentra-tion of lead, chromium, and cadmium, respectively. The specificgrowth rate for A. platensis was 83.33, 94.32, and 98.20% for 0.01mMconcentration of lead, chromium, and cadmium. The specificgrowth rate for A. platensis was 46.66, 43.65, and 45.91% for 0.05mMconcentration of lead, chromium, and cadmium, respectively. Theresults indicate that heavy metals at high concentrations haveconsiderably affected the specific growth rate of the three Arthrospiraspecies. Adsorption of heavy metals is maximal at 0.01mMconcentration compared to 0.05mM concentration. This processis because of the species is subjected tomore stress under high heavymetals concentrations which inhibits the adsorption process.Similar results were in correspondence with the study carried outby Wang and Chen in a pure biological adsorption study using deadbiomass showing a dose dependent growth response [28].Moreover, the specific growth rate of A. indica, A. maxima, and

A. platensis in river water contaminated with tannery effluent was

2 S. Balaji et al.


found to be 54.68, 41.68, and 43.19%, respectively, compared withthe control. These results indicate that Arthrospira species have theability to tolerate heavy metal stress and it can grow in naturalheavy metal contaminated water, which may be attributed to itsbioadsorption capacity. It has also been reported that growth of themicroalgae has a significant factor that influences themetal bindingefficiency [29].

3.2 Chlorophyll content

The impact of heavy metals on TCC of Arthrospira species is shown inFigs. 4–6. Total chlorophyll was extracted with methanol andestimated. When compared with control, the TCC in A. indica wasfound to be 88.88, 85.55, and 95.61% for 0.01mM concentration oflead, chromium, and cadmium, respectively. The TCC in A. indicawas78.75, 77.95, and 79.41% for 0.05mM concentration of lead,chromium, and cadmium, respectively. The TCC in A. maxima was

94, 90.13, and 98.03% for 0.01mM concentration of lead, chromiumand cadmium, respectively. The TCC in A. maximawas 89, 78.06, and84.29% for 0.05mM concentration of lead, chromium, and cadmi-um, respectively. The TCC in A. platensiswas 90, 84.94, and 96.12% for0.01mM concentration of lead, chromium, and cadmium, respec-tively. The TCC in A. platensis was 84.84, 79.14, and 87.49% for0.05mM concentration of lead, chromium, and cadmium,respectively.The TCC of A. indica, A. maxima, and A. platensis in river water

contaminated with tannery effluent was 76.70, 75.89, and 76.65%,respectively, compared with control. A decreased trend in thechlorophyll content was observed in the dose dependent responsewith increased metal ion concentration (Figs. 4–6), whereas agradual increase in the chlorophyll content was observed in thecontrol set, indicating normal function of the photosyntheticenzymes. Similar investigations were carried out previously by Shafiand Agnihotri in Cicer arietinum treated with cadmium and mercury

Figure 1. Specific growth rate of (A) A. indica, (B) A. maxima, and (C) A.platensis at two different concentrations of lead.

Figure 2. Specific growth rate of (A) A. indica, (B) A. maxima, and (C) A.platensis at two different concentrations of chromium.

Bioadsorbent Efficiency of Arthrospira Species 3


showing a dose dependent chlorophyll production [30]. The presentstudy indicates a dose dependent decrease in chlorophyll contentassociated with heavy metal stress. This is due to the result ofinhibition of the enzymes responsible for chlorophyll biosynthesisand tolerance capacity of the species is because of the stimulation ofchlorophyllase activity [31].

3.3 Protein content and biological adsorption ofheavy metals

In general, the protein synthesis in the Arthrospira species is relatedto the metal uptake process. The uptake of metal ions have beendescribed in two stages; the rapid stage at which the metal ions areadsorbed onto the surface of the microorganisms and the slow stagewhere the metal ions are transported across the cell membrane intothe cytoplasm [32, 33]. In the present study, we observed a rapidstage of metal uptake in all three Arthrospira species. It has been

reported that Arthrospira surface contains different functionalgroups such as carboxyl, hydroxyl, sulfate, and other chargedgroups which are created by their protein components that differ intheir affinity and specificity [34, 35]. Heavy metal adsorption couldalso be due to the enhancement of intracellular proline content byArthrospira and making it more resistant to environmental stress[15]. From this report, we understood that the TPC plays a major rolein the adsorption of heavymetals. In the present study, the impact oflead, chromium, and cadmium on TPC in Arthrospira species wasestimated and is shown in Tab. 1. The TPC content was found to bemaximal at lower concentrations (0.01mM) of heavy metals andminimal at higher concentrations (0.05mM). When compared withcontrol, the TPC of A. indicawas found to be 85.71, 75.35, and 79.41%for 0.01mM concentration of lead, chromium, and cadmium,respectively. The TPC of A. indica was 83.33, 66.47, and 74.70% for0.05mM concentration of lead, chromium, and cadmium, respec-tively. The TPC of A. maximawas 92.85, 81.28, and 87.13% for 0.01mM

Figure 3. Specific growth rate of (A) A. indica, (B) A. maxima, and(C) A. platensis at two different concentrations of cadmium.

Figure 4. TCC of (A) A. indica, (B) A. maxima, and (C) A. platensis attwo different concentrations of lead.

4 S. Balaji et al.


Figure 5. TCC of (A) A. indica, (B) A. maxima, and (C) A. platensis at twodifferent concentrations of chromium. Figure 6. TCC of (A) A. indica, (B) A. maxima, and (C) A. platensis at two

different concentrations of cadmium.

Table 1. Effect of various concentrations of lead, chromium and cadmium on TPC of different Arthrospira spp.

Day Control Lead Chromium Cadmium TE

0.01mM 0.05mM 0.01mM 0.05mM 0.01mM 0.05mM

A. indica 1 33� 1.0 30� 0.4 28� 0.7 28� 0.8 26�0.5 31� 0.7 29� 0.5 28� 0.23 43� 0.5 31� 0.5 30� 0.4 29� 0.4 27�0.7 32� 0.4 31� 0.4 30� 0.45 46� 0.7 33� 0.5 31� 1.3 32� 0.5 29�0.1 35� 0.2 33� 0.2 31� 0.511 48� 1.1 36� 1.0 35� 0.7 34� 1.2 31�1.7 37� 1.1 34� 0.7 32� 1.2

A. maxima 1 35� 0.8 31� 0.6 21� 0.6 33� 0.5 30�0.5 34� 0.7 31� 0.4 31� 0.73 42� 1.7 36� 1.2 34� 0.7 34� 0.9 32�0.6 36� 0.9 33� 0.7 33� 0.75 46� 0.8 41� 0.3 36� 0.7 35� 0.2 33�0.7 38� 0.8 36� 0.8 36� 0.611 48� 0.6 42� 0.7 40� 1.2 37� 0.7 35�1.2 41� 1.7 39� 1.2 37� 0.4

A. platensis 1 34� 0.8 32� 0.7 24� 0.7 34� 0.5 31�0.7 33� 0.6 24� 0.7 32� 0.63 43� 1.2 38� 0.2 37� 0.5 35� 0.2 32�0.6 36� 0.5 28� 0.5 36� 0.75 46� 1.4 45� 1.2 39� 1.0 37� 0.2 36�0.4 39� 0.2 31� 0.8 38� 0.511 52� 0.8 48� 0.7 43� 0.5 40� 0.6 39�1.3 40� 0.7 37� 0.4 41� 0.4

The results are presented by mean� SD, n¼ 3. TE, tannery effluent.



concentration of lead, chromium, and cadmium, respectively. TheTPC of A. maxima was 82.69, 76.02, and 81.28% for 0.05mMconcentration of lead, chromium, and cadmium, respectively.The TPC of A. platensis was 87.50, 83.42, and 84.57% for 0.01mMconcentration of lead, chromium, and cadmium, respectively. TheTPC of A. platensis was 85.41, 78.85, and 68.57% for 0.05mMconcentration of lead, chromium, and cadmium, respectively.The TPC of A. indica, A. maxima, and A. platensis in river water

contaminated with tannery effluent was 71.17, 80.11, and 84%,respectively, compared with control. Similar results were observedby Fikriye and Omer in Phaseolus vulgaris when treated with heavymetals [36]. According to the results obtained, the Arthrospira speciescan be employed in the bioadsorption process against lead,chromium, cadmium, and river water contaminated with tanneryeffluent containing thesemetals. In our recent studywith Arthrospiraspecies, we have proved that the biochemical parameters like TCCand TCP play a major role in bioadsorption of zinc and nickel [12].

3.4 Analysis by atomic absorption spectrometry

At the end of the stationary phase, the Arthrospira cell suspensionswere analyzed for theirmetal removal ability. As shown in Tab. 2, themaximum metal removal (lead, chromium, and cadmium) tookplace at lower concentrations (0.01mM) of heavy metals and wasminimal at higher concentrations (0.05mM) of heavy metals. Thepercentage of metal removal ability in the A. indica cell suspensionagainst lead, chromium, and cadmiumwas found to be 83.31, 85.16,and 89.14% for 0.01mM concentration and 76.66, 64.63, and 73.37%

for 0.05mM concentration. Arthrospira maxima cell suspensionshowed 89.45, 93.63, and 83.63% removal ability against lead,chromium, and cadmium for 0.01mM concentration and 73.38,73.38, and 71.81% for 0.05mM concentration. Arthrospira platensiscell suspension showed 83.89, 95.40, and 90.14% removal abilityagainst lead, chromium, and cadmium for 0.01mM concentrationand 74.65, 85.66, and 72.32% for 0.05mM concentration, respective-ly. Similarly, the maximum metal removal ability in river watercontaminated with tannery effluent was 83.24% for A. indica, 86.63%for A. maxima, and 90.14% for A. platensis, respectively. This heavymetal removing ability is because of the saturation of sorption siteson the adsorbent formetal complexion and also due to the chelationof the metal ions by A. platensis [37, 38]. Due to the performance ofheavymetal removal ability of Arthrospira species, it can be employedfor treating industrial effluents.

3.5 Comparison of Arthrospira species bycorrelation analysis

Correlation analysis was performed between TPC with TCC andspecific growth rate for knowing the relationship between thevariables studied. Results are presented in Tabs. 3–5. TCP of A. indica,A. maxima, and A. platensis showed a good positive correlation withspecific growth rate (r2¼ 0.716 for lead, r2¼ 0.862 for chromium,and r2¼ 0.756 for cadmium), whereas TCP showed a moderatepositive correlation with TCC. Correlation analysis suggests thatbioadsorption capacity could be due to the presence of protein andchlorophyll contents that can withstand the stress of lead,

Table 2. Percentage of metal removal by different Arthrospira spp. in atomic absorption spectrometry analysis.

Lead Chromium Cadmium TE

0.01mM 0.05mM 0.01mM 0.05mM 0.01mM 0.05mM

A. indica 83.31% 76.66% 85.16% 64.63% 89.14% 73.37% 83.24%A. maxima 89.45% 73.38% 93.63% 73.38% 83.63% 71.81% 86.63%A. platensis 83.89% 74.65% 95.40% 85.66% 90.14% 72.32% 90.14%

TE, tannery effluent.

Table 3. Comparison among SGR, TCC, and TPC against lead is represented by the correlation coefficient (r2)

A. indica A. maxima A. platensis

SGR TCC TPC SGR TCC TPC SGR TCC TPC

SGR – 0.413 0.716 – 0.428 0.826 – 0.411 0.705TCC 0.413 – 0.616 0.428 – 0.635 0.411 – 0.586TPC 0.716 0.616 – 0.826 0.635 – 0.705 0.586 –

Table 4. Comparison between SGR, TCC and TPC against chromium is represented by the correlation coefficient (r2)



SGR – 0.326 0.862 – 0.321 0.843 – 0.428 0.814TCC 0.326 – 0.732 0.321 – 0.532 0.428 – 0.523TPC 0.862 0.732 – 0.843 0.532 – 0.814 0.523 –

6 S. Balaji et al.


chromium, and cadmium. Specific adsorption of lead, chromiumand cadmium found in this work was comparedwith the outcome ofresults found in the Arthrospira species and it shows that protein andchlorophyll contents are involved in the role of bioadsorptionprocess [18, 29]. The comparison of bioadsorption capacities ofmicroalgae used in this study with those obtained in the literatureshows that all species are more effective for bioadsorption purpose.

4 Conclusions

The aim of this work is to compare bioadsorption characteristics ofthree Arthrospira species for the removal of lead, chromium, andcadmium ions in culture medium and also from river watercontaminated with tannery effluent. From the observed results, it isclear that all three Arthrospira species were found to possess a hightolerance level towards lead, chromium, and cadmium contami-nants and can be considered as potent bioadsorbents due to theirprotective mechanism against the heavy metal stress. This wasobserved through growth, chlorophyll, and protein contents. Theconventional methods for removing heavy metals have severaldisadvantages like continuous input of chemicals, high cost, andtoxicity. In this context, microalgae like Arthrospira species can beused as effective bioadsorbents and also to control pollution againstheavy metals like lead, chromium, and cadmium.

Acknowledgements

The authors are thankful to the management of VIT University forproviding the infrastructure, constant support and encourage-ments. The authors are also thankful to the Technology BusinessIncubator (TBI-VIT), sponsored by the Department of Science andTechnology, for their help in atomic absorption spectrometry.

The authors have declared no conflict of interest.

References0[1] J. C. Igwe, Equilibrium Sorption Isotherm Studies of Cd(II), Pb(II) and

Zn(II) Ions Detoxification from Waste Water Using Unmodified andEDTA-modified Maize Husk, Electron. J. Biotechnol. 2007, 10, 536–548.

0[2] A. Ahmad, R. Ghufran, W. M. Faizal, Cd(II), Pb(II) and Zn(II) Removalfrom Contaminated Water by Biosorption Using Activated SludgeBiomass, Clean – Soil Air Water 2010, 38, 153–158.

0[3] M. M. M. Rahmati, P. Parisa Rabbani, A. Abdolali, A. R. Keshtkar,Kinetics and Equilibrium Studies on Biosorption of Cadmium, Lead,and Nickel Ions from Aqueous Solutions by Intact and ChemicallyModified Brown Algae, J. Hazard. Mater. 2011, 185, 401–407.

0[4] D. Kratochvil, B. Volesky, Removal of heavy metals by a newbiosorbent, in Biotechnology and the Mining Environment, Proceedings ofthe 13th BIOMINET Meeting (Eds.: L. Lortie, P. Bedard, W. D. Gould),Ottawa, Canada 1997, pp. 1–15.

0[5] A. Kapoor, T. Viraraghavan, D. Roy, Removal of Heavy Metals Usingthe Fungus Aspergillus niger, Bioresour. Technol. 1999, 70, 95–104.

0[6] E. Romera, F. González, A. Ballester, M. L. Blázquez, J. A. Muñoz,Comparative Study of Biosorption of Heavy Metals Using DifferentTypes of Algae, Bioresour. Technol. 2007, 98, 3344–3353.

0[7] R. Say, A. Denizli, M. Y. Arıca, Biosorption of Cadmium(II), Lead(II),and Copper(II) with the Filamentous Fungus Phanerochaete chryso-sporium, Bioresour. Technol. 2001, 76, 67–70.

0[8] S. S. Gowd, P. K. Govil, Distribution of Heavy Metals in SurfaceWaterof Ranipet Industrial Area in Tamil Nadu, India, Environ. Monit. Assess.2008, 136, 197–205.

0[9] S. Roy, A. N. Ghosh, A. R. Thakur, Uptake of Pb2þ by aCyanobacterium Belonging to the Genus Synechocystis, Isolated fromEast Kolkata Wetlands, Biometals 2008, 21, 515–524.

[10] K. Chojnacka, Biosorption and Bioaccumulation the Prospects forPractical Applications, Environ. Int. 2010, 36, 299–307.

[11] M. Revathi, M. Saravanan, A. B. Chiya, M. Velan, Removal of Copper,Nickel and Zinc Ions from Electroplating RinseWater, Clean – Soil AirWater 2012, 40, 66–79.

[12] S. Balaji, T. Kalaivani, C. Rajasekaran, Biosorption of Zinc and Nickeland Its Effect on Growth onDifferent Spirulina Species, Clean – Soil AirWater 2013, 41, 1–6.

[13] S. Balaji, K. Gopi, B. Muthuvelan, Production of Poly Hydroxybuty-rates from Cyanobacteria for the Production of Bioplastics, Algal Res.2013, 2, 278–285.

[14] R. K. Aneja, G. Chaudhary, S. S. Ahluwalia, D. Goyal, Biosorption ofPb2þ and Zn2þ by Non-Living Biomass of Spirulina sp., Indian J.Microbiol. 2010, 50, 438–442.

[15] K. Chojnacka, A. Mowoyta, Mechanism of Heavy Metal IonBiosorption by a Blue-Green Alga Spirulina Species, Inz. Chem. Proc.2001, 22, 331–336.

[16] A. Esposito, F. Paganelli, F. Veglio, pH Related Equilibria Models forBiosorption in Single Metal Systems, Chem. Eng. Sci. 2002, 57, 307–313.

[17] N. Das, Remediation of Radio Nuclide Pollutants ThroughBiosorption – an Overview, Clean – Soil Air Water 2012, 40, 16–23.

[18] S. Sayin, A. B. Yilmaz, N. Ergun, F. Turan, Competitive Biosorption ofDifferent Forms of Lead [Pb(NO3)2 and Pb(CH3COO)2] on Growth,Biomass and Proline in Spirulina platensis, Afr. J. Biotechnol. 2011, 10,18458–18462.

[19] C. Zarrouk, PhDS Thesis, Université de Paris, Paris 1966.

[20] P. Rohan Pai, A. Manasa, T. Kalaivani, C. P. Mohammed Ajeesh, C.Rajasekaran, B. N. Prasad, Simplified cost effective media variantsfor the rapid culture of Spirulina platensis, in Recent Advances inBiotechnology (Eds.: B. N. Prasad, L. Mathew), Excel India Publishers,New Delhi 2008, p. 129.

[21] H. Chen, S. S. Pan, Bioremediation Potential of Spirulina: Toxicityand Biosorption Studies of Lead, J. Zhejiang Univ. Sci. 2004, 6, 171–174.

[22] V. K. Gupta, R. Arshi, V. K. Saini, J. Neeraj, Biosorption of Copper(II)from Aqueous Solutions by Spirogyra Species, J. Colloid Interface Sci.2006, 296, 59–63.

[23] T. R. Parsons, J. D. H. Strickland, Discussion of SpectrophotometricDetermination of Marine-plant Pigments, with Revised Equations forAscertaining Chlorophylls and Carotenoids, Yale University Press, NewHaven, CT 1963.

Table 5. Comparison between SGR, TCC and TPC against cadmium is represented by the correlation coefficient (r2)



SGR – 0.582 0.761 – 0.316 0.912 – 0.414 0.756TCC 0.582 – 0.648 0.316 – 0.438 0.414 – 0.685TPC 0.761 0.648 – 0.912 0.438 – 0.756 0.685 –



[24] O. H. Lowry, N. J. Rosenbrough, A. L. Farr, R. J. Randall, ProteinMeasurement with the Folin Phenol Reagent, J. Biol. Chem. 1951, 193,265–275.

[25] American Public Health Association (APHA), Standard Methods forExamination of Water and Wastewater, 20th Ed., American PublicHealth Association, Washington, DC 1998.

[26] D. R. Row, I. M. Abdel-Magid, Handbook of Waste Water Reclamation andReuse, CRC Press, Boca Raton, FL 1995.

[27] S. R. Mousavi, M. Balali-Mood, B. Riahi-Zanjani, H. Yousefzadeh, M.Sadeghi, Concentrations of Mercury, Lead, Chromium, Cadmium,Arsenic and Aluminum in Irrigation Water Wells and WastewatersUsed for Agriculture in Mashhad, Northeastern Iran, Int. J. Occup.Environ. Med. 2013, 4, 80–86.

[28] J. Wang, C. Chen, Biosorption of Heavy Metals by Saccharomycescerevisiae, Biotechnol. Adv. 2006, 24, 427–451.

[29] E. Wilde, J. R. Benemann, Bioremoval of Heavy Metals by the Use ofMicro Algae, Biotechnol. Adv. 1993, 11, 781–812.

[30] M. Shafi Tantrey, R. K. Agnihotri, Chlorophyll and Proline Content ofGram (Cicer arietinum L.) under Cadmium and Mercury Treatments,Res. J. Agric. Sci. 2010, 1, 119–122.

[31] Y. C. Lee, S. P. Chang, The Biosorption of Heavy Metals from AqueousSolution by Spirogyra and Cladophora Filamentous Macroalgae,Bioresour. Technol. 2011, 102, 5297–5304.

[32] D. T. Swift, D. Forciniti, Accumulation of Lead by Anabaena cylindrica:Mathematical Modelling and an Energy Dispersive X-ray Study,Biotechnol. Bioeng. 1997, 55, 408–419.

[33] B. Volesky (Ed.), Biosorption and biosorbents, in Biosorption of HeavyMetals, CRC Press, Boca Raton, FL 1990, pp. 3–5.

[34] P. S. P. Alia, P. Mohanty, Proline in Relation to Free RadicalProduction in Seedlings of Brassica juncea Raised under SodiumChloride Sstress, Plant Soil 1993, 155, 497–500.

[35] N. Rangsayatorn, P. Pokethitiyook, E. S. Upatham, G. R. Lanze,Cadmium Biosorption by Cells of Spirulina platensis TISTR 8217Immobilized in Alginate and Silica Gel, Environ. Int. 2004, 30,57–63.

[36] K. Z. Fikriye, M. Omer, Effects of Some Heavy Metals on Content ofChlorophyll, Proline and Some Antioxidant Chemicals in Bean(Phaseolus vulgaris) Seedlings, Acta Biol. Cracoviensia Ser. Bot. 2005, 47,157–164.

[37] M. Jain, V. K. Garg, K. Kadirvelu, Chromium Removal from AqueousSystem and Industrial Wastewater by Agricultural Wastes, Bioremed.J. 2013, 17, 30–39.

[38] G. Dounmez, Z. Aksu, Removal of Chromium(VI) from SalineWastewaters by Dunaliella Species, Proc. Biochem. 2002, 38, 751–762.

8 S. Balaji et al.


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Arthrospira ( Spirulina ) Species as Bioadsorbents for Lead, Chromium, and Cadmium - a Comparative Study