Uptake of uranyl ions from uranium ores and sludges by means of Spirulina platensis, Porphyridium cruentum and Nostok linckia alga

Bioresource Technology 118 (2012) 19–23

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Uptake of uranyl ions from uranium ores and sludges by means of Spirulina platensis, Porphyridium cruentum and Nostok linckia alga Alexandru Cecal a, Doina Humelnicu a,⇑, Valeriu Rudic b, Liliana Cepoi b, Dumitru Ganju a, Angela Cojocari b a b

‘‘Al.I. Cuza’’ University, Faculty of Chemistry, 11-Carol I Bld., 700506 Iasi, Romania Institute of Microbiology, Chishinau, 1-Academiei Str., Science Academy, Republic of Moldova

h i g h l i g h t s " Removal of uranyl ions from the effluents resulting from nuclear technologies by algae. " Investigation of the biosorption of uranyl ions leached from ores and uranium deposits. " Investigation of the biosorption of uranyl ions in sludges resulted from the nuclear processes.

a r t i c l e

i n f o

Article history: Received 7 March 2012 Received in revised form 7 May 2012 Accepted 11 May 2012 Available online 18 May 2012 Keywords: Biosorption Uranyl ions Biomass Isotherms

a b s t r a c t In this paper was studied the uranyl ions biosorption on three types of alga: Nostok linckia, Porphyridium cruentum and Spirulina platensis. These ions were supplied either from a pure solution of uranyl nitrate, or after leaching process of uranium ore, or from the sludge resulting in the output of pure UO2 technology. It was investigated the retention degree versus contact time and afterwards the Langmuir and Freundlich biosorption isotherms of uranyl ions on the three alga types. The retention of UO2þ 2 ions on alga was proved through FTIR spectra plotted before and after biosorption processes. From the experimental data it was found that regardless of origin of uranyl ions, the retention degree on alga decreased in the series.

Spirulina platensis > Porphyridium cruentum P Nostok linckia: Ó 2012 Elsevier Ltd. All rights reserved.

1. Introduction The use of alga, bacteria or hydrophyte plants in the treatment of contaminated effluent with uranyl ions, which come either from uranium ore mines and deposits or by sludges resulting from pure UO2 processing, has concerned a number of researchers (Ashley and Roach, 1990; Francis et al., 1991; Guibal et al., 1992; Hu et al., 1996; Yang and Volensky, 1999). Vogel et al. (2010) studied the biosorption of UO2þ 2 ions by Chlorella vulgaris green algae, stating that the process depends on the pH of the biological medium, uranium concentration and biomass-solution contact time. The retention degree of uranyl ions on the algae was between 45% and 90%, depending on experimental conditions.

⇑ Corresponding author. Tel.: +40 232201136; fax: +40 232201313. E-mail address: [email protected] (D. Humelnicu). 0960-8524/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.biortech.2012.05.053

The removal of uranyl ions from the effluents resulting from nuclear technologies through the use of yeast brewery in different working conditions concerned some research groups (Lin et al., 2004; Liu et al., 2010; Popa et al., 2003; Riodan et al., 1997; Tykva et al., 2009). Francis and Dodge (1998) investigated the possibility of remediation of soil and water contaminated with uranium and toxic metals, using the three working methods, namely the selective extraction, biodegradation and photodegradation of chemical compounds which appeared. Firstly, there were extracted these metal ions from corresponding pollution area with citric acid solution, and then the resulting complex compounds were subjected to biodegradation by Pseudomonas fluorescens. Since the uranyl citrate resisted to the biodegradation, it was subject to the UV photodegradation. Finally, by alkaline precipitation, uranium recovered as UO3xH2O. The interaction of uranyl ions from different contaminated areas with the bacterial strains, Paenibacillus sp. JG-TB8 and

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A. Cecal et al. / Bioresource Technology 118 (2012) 19–23

Sulfolabus oxidocaldartius DSM 639 were studied by Reitz et al. (2008). Using the X-ray studies absorption spectroscopy (XAS), there was found an interaction mechanism by coordination of uranyl ions to the biochemical compounds of living cells. Parson et al. (2006) investigated the adsorption of U(VI) on inactivated cells of Alfalfa biomass by inductively coupled plasma optical emission spectroscopy and X-ray absorption spectroscopy, pointing out that the carboxyl functional groups of biochemical compounds of living cells retain UO2þ 2 ions by complexation. Dienemann et al. (2008) used separate columns filled with alga: Cladophora fracta, Cladophora glomerata and Cladophora aegagrapila to purify the water contaminated with UO2þ 2 , proposing a biosorption mechanism of these ions on given biomass. U(VI) and Th(IV) biosorption onto Ulva gigantea and its modified form with glutaraldehyde, in several experimental conditions was accomplished by Bozkurt et al. (2011). There are plotted the biosorption isotherms and are accounted the values of kinetic and thermodynamic parameters to characterize the retaining of these heavy metals on these biomasses. Similar studies for uranium uptake by means of a composite: Ulva sp – sepiolite are reported by Donat et al. (2009). Shawky et al. (2005) used water hyacinth plant for biosorption of uranium as a pollutant metal for the environment. Other authors reported the removal of radionuclides as: 90Sr and 226Ra, using some bacteria strains, as microbiological collectors: Oscillatoria homogenea cyanobacterium (Dabbagh et al., 2007) or Chromobacterium, Chrsyseobacterium and Corynebacterium (Satvatmanesh et al., 2003) in several contaminated areas. Cecal et al. (1997a, 1997b, 2000) studied the biosorption and 4+ bioaccumulation of UO2þ ions, but also the other radioca2 and Th tions of contaminated effluents coming from industrial or research laboratories in the nuclear field, using alga: Scenedesmus quadricauda, Nostok linckia, Spirulina platensis, Porphyridium cruentum, Tolyprotix. In this paper it is investigated the biosorption of uranyl ions leached from some uranium ores and uranium deposits, as well as those contained in sludges resulted from the output process of nuclear pure uranium dioxide, on the algal biomasses: S. platensis, P. cruentum and N. linckia in different experimental conditions. The results are compared with those obtained in the biosorption of the same ions contained in a pure solution of UO2(NO3)2.

Table 1 Concentrations of most important elements in solutions obtained after macerations of the ores (U-C) or of sludge (U-R). Sample

U-C U-R

Conc. (mg/L) Fe

Ni

Co

Ca

Mn

Cr

Zn

1604.5 1193.1

36.9 11.7

24.3 2.5

1227.2 1090.5

210.2 20.4

4.2 1.2

252.7 48.2

Note: The uranium concentration of the two samples was: for U-C: 0.012 M, for U-R: 0.0097 M, respectively.

The chemical compositions in elements (except uranium) of the two solutions resulted after filtrations were determined by atomic absorption spectrometry. The concentrations of uranyl ions were established spectrophotometrically by Arsenazo III method. The values obtained from these measurements are given in Table 1. The concentration of elements as different metals contained both in uranium ores and sludge, was measured from solutions by flame atomic absorption spectroscopy (FAAS) using a Continuum Source Atomic Absorption Spectrometer – ContrAA-300 having a high resolution Echelle double monochromator. Then there was prepared an aqueous solution of pure UO2(NO3)2 having the concentration 102 mol/L, to start a comparative study of UO2þ 2 ions retaining on the same algal biomass, in the absence of such as microelements. 2.2. Preparation of algal biomass Green alga S. platensis and N. linckia and red algae P. cruentum were grown in Institute of Microbiology Chishinau of Science Academy of Moldova Republic, in the nutrient medium having a commonly composition of chemicals: MgSO4, Ca(NO3)2, KCl, NaCl, K2HPO4, NaNO3, EDTA etc. (Cojocari, 2006; Rudic, 1993). The biochemical composition of the three types of alga established in the Institute of Microbiology – Chishinau after literature indications (Rudic et al., 2007) is shown in Table 2. These alga were used in the form of suspension being subject to continuous illumination at a light flux: U = 3.6  103 J cm2 s1. 2.3. Conducting laboratory experiments

2. Methods Experimental research considered two directions, namely: The chemicals UO2(NO3)26H2O, HCl, HNO3, and Arsenazo-III were purchased in analytical purity. All chemicals were used without any further purification in the experiments. 2.1. Leaching of uranyl ions from ores or sludges Firstly it tried to bring the uranium in soluble form as UO2þ 2 ions from both uranium ores or sludges resulting from the output of pure UO2. For this purpose there were taken separately about 0.5 kg of ore and sludge, respectively, which were placed in porcelain capsules, and aqua regia to completely cover each solid mass was poured. The process of maceration in aqua regia (3 vol. HClconc. + 1 vol. HNO3conc.) took place 72 h with intermittent shaking. Then the resulted acid suspension was diluted with 10 vol. of distilled water for extraction of UO2þ 2 and other metal ions as microelements in the liquid phase. By vacuum filtration and washing with water, it was able to separate the residue of SiO2 and then the yellow–brown filtrate was retained for the further experiments. Afterwards, NH4OH solution (25%) was used to adjust the pH to a value of 3.5 inside of filtrate, without removing the most of other metals such iron, as Fe(OH)3 at pH > 3.5.

1. To follow retention in several time intervals of uranyl ions in the same quantity of biomass. 2. To study of uranyl ions biosorption on different amounts of alga, at a predetermined contact time. In the cylindrical glass vials of 100 mL capacity there were poured 25 mL of solution containing uranyl ions from pure nitrate, ore or sludge previously prepared, over which there were added

Table 2 The biochemical composition of microalga biomass. Substances groups

Specium Porphyridium cruentum % BAU

Spirulina platensis % BAU

Nostok linckia % BAU

Proteins Glucids Lipids Carotenoids Ficobilins Nucleic acids Glycerol

28–35 17–22 0.5–0.8 3–7 5–7 3–4 –

65–70 10–15 3–5 0.4–0.6 5–9 3–4 2–4

15–25 35–50 0.5–2 0.5–1.0 3–7 2–3 0.1–0.5

21

100 90 80 70 60 50 40 30 20 10 0

U-pure U-C U-R

0

0.5

1

2

24

48

contact time, h Fig. 2. Variation in time of the retention degree of uranyl ions on Spirulina platensis algae.

90

U-pure

80

U-C

70

U-R

60

R, %

different amounts of suspension of alga S. platensis, N. linckia and P. cruentum with nutrient medium, and distilled water so that the total volume of solution from each sample to be 40 mL. In parallel was determined the quantities of dried alga in a volume of 15 mL suspension, so that measurements of uranyl ions retention relates to gram of solid biomass. Every time interval, the samples were centrifuged (3000 rotations/min) for separation of solid biomass from solution. Then, from the resulting solutions after centrifugation 5 mL were taken out, to determine the concentrations of uranyl ions by UV–vis spectrophotometry, applying the method with Arsenazo III (Savvin, 1961). The absorbance values were obtained on a spectrophotometer UV-2100 Cole-Parmer Spectrophotometer at a wavelength of 660 nm and the respective ion concentrations were determined from a calibration line after Lambert–Beer equation. The experimental obtained data were used in drawing plots that represent the retention degree in time of uranyl ions on alga and Langmuir and Freundlich biosorption isotherms of the same ions in different amounts of biomass for the same contact time UO2þ 2 ions solution – algae. There have also been plotted FT-IR spectra of pure alga: S. platensis and P. cruentum, and of the same biomass after retaining of uranyl ions from pure UO2(NO3)2, using a device type ALPHA Bruker spectrophotometer in a KBr thin disk. The dry algal biomass mixed with KBr and pressed into a tablet form. The FT-IR spectrum was then recorded for each prepared sample.

R, %

A. Cecal et al. / Bioresource Technology 118 (2012) 19–23

50 40 30 20 10 0 0

0.5

1

2

24

48

contact time, h

3. Results and discussion

Fig. 3. Dependence of retention degree on contact time between uranyl ions and Porphyridium cruentum algae.

The retention degree (R) of uranyl ions by each algae, at different intervals of contact time was calculated with the Eq. (1):

R¼

C0  C  100; C0

ð1Þ

%

where C0 and C mean the concentrations of uranyl ions at initial time and after a certain contact time with biomass as adsorbent, expressed in mmol/L. Practical results obtained for the studied systems are presented in the Figs. 1–3 in the coordinates: R = f(t) were plotted for each algae: N. linckia, S. platensis and P. cruentum. Afterwards, using the obtained data from the studied systems for 24 h contact time only, the Langmuir and Freundlich biosorption isotherms were investigated. Thus, the Langmuir biosorption isotherms were drawn by plotting the experimental data in coordinates 1/q = f(1/C) corresponding to the Eq. (2):

1 1 1 ¼ þ q q0  K L  C q0

80

U-C

60 50 40 30 20 10 0

0.5

C0  C  V; m

mmol=g

ð3Þ

Here V and m represent the volume of solution containing uranyl ions (L) and amount of the dry biomass (g), respectively. Between the saturation capacity (q0) and the uranium capacity reached at equilibrium (qm) in a saturated monolayer of UO2þ 2 ions formed on the algae surface a following relation can be written:

qo ¼ qm

K L  C eq 1 þ K L  C eq

ln q ¼ ln K F þ

U-R

0

q¼

ð4Þ

where Ceq means the ions concentration at the equilibrium state. On the other hand the biosorption isotherms of Freundlich type resulted by plotting the experimental data in coordinates: ln q = f (ln C), concerning to the following equation, written in logarithmic form:

U pure

70

R, %

ð2Þ

From the crossing of the straight lines with ordinate axis the q0 saturation capacity is calculated and from the respective slopes result the bond energy value (KL) of metal ion retained by solid mass. In Eq. (2) q means the amount of the retained metal ions on biomass (mmol/g dry algae):

1

2

24

48

ð5Þ

In this relation q and C mean the same parameters as in the case of Langmuir isotherms. The KF and n constants signify biosorption capacity, respectively the intensity of biomass retention of metal ions in connection to the sorbent surface heterogeneity. From the crossing with ordinate axis of each line, the value of KF may be accounted, while the n parameter can be calculated from its slope:

contact time, h

tg a ¼ Fig. 1. Time dependence of retention degree of uranyl ions on Nostok linckia algae.

1 ln C n

1 n

ð6Þ

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A. Cecal et al. / Bioresource Technology 118 (2012) 19–23

1/q, g algae/mmol

0.7

y = 0.0425x + 0.0735 R2 = 0.9671

U-pure

0.6

U-C

0.5

U-R y = 0.0209x + 0.017 R2 = 0.9895

0.4 0.3 0.2

y = 0.0105x + 0.0047 R2 = 0.8542

0.1 0 0.127

0.14

0.162

0.189

0.193

0.196

1/C, L/mmol Fig. 4. Langmuir isotherms for biosorption of the uranyl ions on Nostok linckia.

U-pure

3.5

y = 0.1294x + 1.0308 R2 = 0.9445

U-C

3

U-R

y = 0.1455x + 1.4919 R2 = 0.9654

ln q

2.5 2 1.5

y = 0.1381x + 0.0702 R2 = 0.9824

1 0.5 0 1.504

1.625

1.651

1.723

1.875

1.962

ln C Fig. 5. Freundlich isotherms for biosorption of the uranyl ions on Nostok linckia.

As examples, the Langmuir and Freundlich biosorption isotherms for the uranyl ions retained on the N. linckia are presented in the Figs. 4 and 5. The obtained results from the processing experimental data are presented in Table 3. The constants values of: qm, KL, KF and n obtained by processing of biosorption isotherms Freundlich and Langmuir and presented in Table 3, are in good agreement with data provided by other authors (Chojnacka, 2007; Gokhale et al., 2008) that investigated the retention of some ions on algae: Cr3+ Cu2+, Cd2+, Zn2+, Mn2+, CrO42, etc. in different experimental conditions. The Langmuir (qm) and Freundlich (KF) adsorption constants can be used to compare the biosorption process of metal ions on the several biomasses. Thus, for higher qm and smaller KF values the biosorption process is stronger. That means that biosorption of UO2þ ions from pure solutions of UO2(NO3)2 on algal biomass, is 2 higher than for the U-C and U-R samples, which contains some microelements.

Furthermore the biosorption of uranyl ions from the leached uranium ore (U-C) is slower than for the same ions resulted from the sludge (U-R), even if UO2þ 2 concentration is smaller in the latter case than for first one. It is possible that metal ions (as microelements) present in ore (U-C) and sludge (U-R) to have a role in bioaccumulation of uranyl ions on the three alga hindering more or less the retention of these ions as simple UO2þ or in several complex compounds (Christen 2 and Meyer, 1997). Consequently, where the concentration of metal ions is higher (U-C) the inhibiting effect on algae biosorption of uranyl ions is stronger than in the other case (U-R). On the other hand, the higher are the values of n, the much more the binding sites on the biomass surface for retaining of metal ions are involved and the depollution effect becomes stronger. FT-IR spectra supply some additional information on the uranyl ions biosorption on the different biochemical components of these algae.

Table 3 The obtained parameters from the Langmuir and Freundlich biosorption isotherms, at 298.15 K. Algae type

Nostok linckia

Spirulina platensis

Porphyridium cruentum

Sample

U-pure U-C U-R U-pure U-C U-R U-pure U-C U-R

Langmuir

Freundlich

R2

qm (mmol/g)

KL (L/mmol)

R2

KF (mmol/g)

n

0.854 0.967 0.989 0.992 0.920 0.775 0.988 0.990 0.982

30.90 12.56 17.61 64.28 43.12 52.22 51.04 43.97 46.60

0.44 0.73 0.62 0.53 0.81 0.72 0.48 0.67 0.55

0.944 0.982 0.965 0.973 0.918 0.863 0.984 0.953 0.984

4.96 6.82 5.20 1.05 1.38 1.26 3.69 4.28 3.89

6.72 5.84 6.27 8.32 7.13 8.05 6.06 5.47 5.85

A. Cecal et al. / Bioresource Technology 118 (2012) 19–23

The analysis of the FTIR spectra points out different positions corresponding to several vibration bands of functional groups from the biochemical components of algae before and after biosorbtion of uranyl ions. As a result the bands by vibration for functional groups are shifted (Wang and Chen, 2009). (a) @C@O in fatty acids, esters and protein: between 1780 and 1730 cm1, or ketones in the carbohydrates: 1690– 1660 cm1. (b) „C–NH2 and @C@N–H in protein and nucleic acids: 1650– 1620 and 1360–1030 cm1. (c) –OH in carbohydrates: 1400–1340 cm1. Also there are affected other functional groups such as: @S@O: 1070–1030 cm1, „C–H: 970–885 cm1, „C–S–: 705–550 cm1 and others. It is stated that no vibrational bands were found for classical metal–ligand bound below 400 cm1. Taking into account the results carried out from Langmuir and Freundlich isotherms (Table 3), the biochemical composition of these alga (Table 2) and FTIR spectra, it can be seen that the biosorbtion of uranyl ions on alga decreases as follows:

Spirulina platensis > Porphyridium cruentum P Nostok linckia;

especially based on higher proteins contents and lipids of the first biomass. It still cannot be underestimated the contribution of carbohydrates to biosorption of uranyl ions, but it can be considered less intense in the studied systems. 4. Conclusions 1. Taking into account the time-increasing of retaining degree and the values of parameters from the Langmuir and Freundlich isotherms, it was established some differences concerning the uptake of UO2þ ions on alga in the given experimental 2 conditions. 2. The vibration bands in FTIR spectra showed that the corresponding functional groups of proteins, carbohydrates from biomasses composition are shifted due to the retained uranyl ions. Inside of living cells perhaps appeared weak interactions between biochemical compounds of the studied algae and the UO22 + ions. 3. The proposed alga can be used to purify wastewater polluted with uranium ions.

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