Gold biosorption by exopolysaccharide ... - Wiley Online Library

Journal of Applied Microbiology ISSN 1364-5072

ORIGINAL ARTICLE

Gold biosorption by exopolysaccharide producing cyanobacteria and purple nonsulphur bacteria G. Colica, S. Caparrotta, G. Bertini and R. De Philippis Department of Agricultural Biotechnology, University of Florence, Firenze, Italy

Keywords biosorption, exopolysaccharide-producing cyanobacteria, gold biorecovery, precious metal uptake, purple nonsulphur bacteria. Correspondence Roberto De Philippis, Department of Agricultural Biotechnology, University of Florence, Piazzale delle Cascine 24, I – 50144 Firenze, Italy. E-mail: [email protected] 2012/1044: received 9 June 2012, revised 28 August 2012 and accepted 3 September 2012 doi:10.1111/jam.12004

Abstract Aims: This study was aimed at investigating the possible exploitation of phototrophic micro-organisms for the removal and the recovery of Au from Au-containing wastewaters deriving from a plating industry. Methods and Results: A screening among ten phototrophic micro-organisms was carried out with pure solutions of Au to select the best strain in terms of metal uptake and selectivity. The direct use of the selected micro-organism on the Au-containing industrial wastewater was then carried out with the aim of assessing the potential of its use for the removal and the recovery of the precious metal from industrial wastewaters. Conclusions: This study showed the good potential of some exopolysaccharide-producing cyanobacteria as biosorbents for the recovery of Au from wastewaters of plating industries but also pointed out the need to design an efficient technology for the recovery of the metal from the biomass. Significance and Impact of the Study: The selection of good biosorbents for the recovery of gold from industrial wastewaters may open new perspectives to a green biotechnology so far considered too expensive for the mere treatment of wastewaters containing low valuable metals.

Introduction Gold is a precious metal extensively used not only in jewellery but also for high technological uses in nanotechnology, medicine, aero space industry and in many other applications that require the high reliability of this metal (Anon. 2009). As a consequence, gold recovery from leaching solutions (Volesky 2003), electronic scrap (Rhee et al. 1995; Cui and Zhang 2008) and electroplating wastewaters (Syed 2012) is becoming an important issue. The recovery of gold from dilute solutions generally involves zinc-dust precipitation, carbon adsorption or solvent extraction (Syed 2012). Alternative recovery processes based on ion-exchange resins also received specific attention (Leao and Ciminelli 2000; Syed 2012) but, in most cases, the high costs of these technologies limited their use. A number of investigations have focused on gold recovery and mining processes carried out using biosorbents such as algae (Kuyucak and Volesky 1989; Mack et al. 2007; Chakraborty et al. 2008; Mata et al. 2008) and micro-organisms (Niu and Volesky 2000; 1380

Tsuruta 2004; Lin et al. 2005; Das 2010), but among them only few reports appeared on the biosorption of gold ion with cyanobacteria (Savvaidis 1998; Lengke et al. 2006; Chakraborty et al. 2008). It is well known that three main mechanisms are involved in the biological process of metal uptake from aqueous solutions (Darnall et al. 1986; Chong and Volesky 1995): (i) the adsorption of metal ions onto the surface of microbial cells (biosorption), (ii) the intracellular uptake of metal ions and (iii) the chemical transformation of metal ions by micro-organisms. The biosorption has been reported to be the fastest mechanism, thus it is considered the most promising for metal sorption and recovery from wastewaters (Volesky 2003). The cell surface of micro-organisms consists of polysaccharides, proteins and lipids that within the wall provide the amino, carboxylic, sulphydryl, phosphate and thiol groups capable of binding metals (Volesky 2003). Carboxyl groups are considered the main binding sites both in the cell wall of gram-positive bacteria (Gadd and White 1993) and in cyanobacteria (De Philippis et al.

Journal of Applied Microbiology 113, 1380--1388 © 2012 The Society for Applied Microbiology

G. Colica et al.

2011), even if an important role was also attributed to the amino groups of the outermost cell layers (Crist et al. 1981; Ting et al. 1991; Micheletti et al. 2008b). The different abundance and spatial distribution of these groups on the cell surface are considered the main cause of the differences observed in the efficiency and in the selectivity of the metal adsorption by different microbial strains (Hammouda et al. 1995; Tsuruta 2004; De Philippis et al. 2007; Micheletti et al. 2008a,b). A number of exopolysaccharide (EPS)-producing cyanobacteria showed very good metal sorption performances towards different types of metal cations (De Philippis et al. 2011). It was in particular suggested that these good performances originated from the high density of negative charges on the EPS surrounding the cyanobacterial cells, which is due to the presence of uronic acids and sulphate groups in the macromolecules (De Philippis et al. 2011). Recently, interesting biosorption performances towards Ruthenium were reported for a selected strain of Rhodopseudomonas palustris (Colica et al. 2012). Moving from these considerations, this study was aimed at investigating the possible exploitation of phototrophic micro-organisms, namely EPS-producing cyanobacteria and purple nonsulphur bacteria (PNSB), for the removal and the recovery of Au from Au-containing wastewaters of a plating industry. As a first step, a screening among several phototrophic micro-organisms was carried out to select the best strain in terms of metal uptake and selectivity. For this purpose, pure solutions of Au and of the main metals contaminating the wastewaters of the Au plating process investigated were used. As a second step, the selected micro-organism was directly used on the Au-containing industrial wastewater to assess its potential for being utilized in the removal and the recovery of the precious metal from the wastewaters. Materials and methods Micro-organisms utilized Ten phototrophic micro-organisms were tested, six PNSB (R. palustris strains 42OL, SC0, AV32a, AV33, CGA009 and Rhodobacter sphaeroides strain AV1) and four EPSproducing cyanobacteria (Cyanothece sp. strains 16Som2, CE4, VI22 and Nostoc sp strain PCC7936). All the strains utilized in this study, except Nostoc PCC7936 and R. palustris CGA009, belong to the culture collection of the Department of Agricultural Biotechnology, University of Florence, Italy, and are freely available, upon request to the Corresponding Author, for scientific purposes. Nostoc PCC7936 is available at the Pasteur Culture Collection, France, while R. palustris CGA009 was a kind gift of Prof Caroline S. Harwood, Washington State Univer-

Gold biosorption with phototrophs

sity, Seattle, USA. According to their nutritional requirements, PNSB were cultivated in RPN medium (Bianchi et al. 2010), Cyanothece VI22, CE4 and 16Som2 in enriched seawater medium (AMA, De Philippis et al. 1993) and Nostoc PCC7936 in BG 110 medium (De Philippis et al. 2000). Metal solutions utilized For the first set of experiments (screening of the strains), pure solutions separately containing Au, Cu, Zn or Ni (20 mg l1), obtained by diluting AA standard solutions at 1000 mg l1 (Sigma-Aldrich, St Louis, MO, USA), were utilized at a pH of 40. For the second set of experiments, an industrial wastewater containing (mg l1) Au (28280), Cu (450), Zn (30) and Ni (28610) at pH 42 was used. The chemical species of Au in solution was Au (III) chloride. Removal tests using mono-metal solutions The tests were carried out by adding 2 ml of microbial cultures, sampled during the stationary phase, to 13 ml of mono-metal solutions in 15-ml tubes. Blanks prepared by adding 2 ml of culture medium devoid of cells to 13 ml of metal solutions were used. After 72 h, the samples were centrifuged at 3500 g for 20 min in order to remove the microbial biomass from the solution and to analyse the concentration of the metals remained in solution. All the experiments were carried out in quintuple and the results are reported as mean values ± standard deviation. Removal tests using industrial Au-containing wastewaters The tests were carried out by confining the biomass in dialysis tubings (cut off 16 000 Da, Ø 286 mm) that were subsequently dipped in the wastewater for 72 h. The biomass was utilized with or without an acid pretreatment. For the acid pretreatment, an aliquot of the bacterial culture was confined in dialysis tubing and dipped in a 03% HCl solution for 6 h in order to remove the metal ions possibly bound to the negatively charged groups of the exocellular polysaccharidic layers (Micheletti et al. 2008a). Subsequently, the confined biomass was dialysed against deionized water for 24 h to remove the excess of acid. After this treatment, 50 ml of the pretreated cultures, at a biomass concentration of about 1 g (dry weight) l1, was confined in dialysis tubings (cut off 16 000 Da, Ø 143 mm) which were dipped in 450 ml of industrial wastewater for 72 h under continuous stirring. The final pH of the metal solution


1381


G. Colica et al.

was adjusted to 40. Blanks were prepared by confining 50 ml of culture medium devoid of cells in dialysis tubings. The tubings were subsequently dipped in the 450 ml of wastewater for 72 h. Use of Cyanothece 16Som2 biomass for Au biosorption from industrial wastewaters For the tests on Au bioremoval from industrial wastewaters, a culture of Cyanothece 16Som2, at a biomass concentration of 117 g dry weight l1, was prepared in three different ways before being added to 3 l of the industrial wastewaters. In test L1, 8 l of culture was directly added to the metal solution. In test L2, 8 l of culture was first dialysed against deionized water for 24 h and then concentrated in an oven at 40°C to a final volume of 1 l before being added to 3 l of the industrial wastewaters. In test L3, 8 l of culture was prepared as in test L2 but the concentration of the culture was carried out at 100°C. At the end of the contact time between the biomass and the wastewater (72 h), aliquots of the cell suspensions were centrifuged at 3500 g for 20 min at 20°C to remove the microbial biomass before carrying out the analyses of the metal content of the solutions. Recovery of Au from the biomass After the contact with the Au-containing wastewater, the biomass was recovered by centrifugation (3500 g for 20 min at 20°C), and the pellet was incinerated in an oven at 1200°C for 1 h. The ashes obtained at the end of this treatment were analysed for determining their content in metals by Scanning Electron Microscopy and Energy Dispersive Spectroscopy (SEM/EDAX). Analytical methods The concentration of metals present in solution before and after the contact between metal solutions and the biomass was determined by an Atomic Adsorption Spectrometer (AAS) (Aanalyst 400; Perkin Elmer, Waltham, MA, USA). The metal uptake at the equilibrium qe, expressed as mg of metal removed per g of dry biomass, was calculated as: qe ¼

VðCi Cf Þ m

where V is the sample volume (l), Ci and Cf are the initial and final metal concentrations (mg l1), respectively, and m is the amount (g) of dry biomass utilized (Volesky and May-Phillips 1995). In the experiments, Ci was calculated taking in consideration the metal removal observed in controls carried out without the biomass. 1382

The concentration of the biomass was determined as dry weight (g l1) by filtering 10 ml of the cell suspension on 045 lm filters and by drying the filters at 100°C until constant weight. The elemental composition of the ashes was determined by Scanning Electron Microscopy and Energy Dispersive Spectroscopy (SEM/EDAX) with a SEM (Philips 515, Eindhoven, The Netherlands) coupled to an Energy Dispersive Spectrometer (EDAX Inc. Mahwah, NJ, USA). The concentration of Au in the samples was measured using electron probe microanalysis performed at 25 kV accelerating voltage, and with an accumulation of X-radiation for 40 s. Results Determination of Au, Cu, Zn and Ni biosorption performances of selected cyanobacteria and PNSB In a preliminary screening, four cyanobacteria and six PNSB were tested for their metal uptake capability using pure solutions of Au and of Cu, Ni and Zn, the three metal contaminants most frequently found in Au wastewaters. The highest Au uptake was observed with Cyanothece CE4, Cyanothece 16Som2 and Cyanothece VI22, which showed q values of 318 ± 42, 164 ± 20 and 115 ± 18 mg g1, respectively (Fig. 1). Among the other metals tested, Cu was the metal sorbed at the highest q values, while Zn and Ni were removed at much lower q values and not by all the strains (Fig. 1). The best Cu uptake performances were observed with Cyanothece 16Som2, R. palustris SC0 and R. palustris CGA, which showed q values of 201 ± 20, 146 ± 21 and 125 ± 20 mg g1, respectively. The highest q values towards Ni were 58 ± 3, 50 ± 3 and 34 ± 2 mg g1 with Cyanothece 16Som2, Cyanothece CE4 and Cyanothece VI22, respectively. With respect to Zn, all the strains tested showed very low, if any, q values, with the only exception of Cyanothece CE4 that showed a Zn uptake of 69 ± 10 mg g1. Metal removal laboratory tests of selected microbial strains on Au-containing wastewater The three micro-organisms that showed the best performances in Au removal from monometal solutions were tested, with or without an acid pretreatment, against an industrial Au-containing wastewater. In the experiments carried out with untreated biomass (Fig. 2), Cyanothece 16Som2 showed a q value towards Au of 164 ± 2 mg g1 while Cyanothece VI22 and Cyanothece CE4 showed q values of 146 ± 2 and 52 ± 1 mg g1, respectively. The three cyanobacteria also removed Ni from the wastewater at q values of 214 ± 2, 140 ± 2 and 90 ± 2 mg g1 for


G. Colica et al.


360 340 320 mg of metal removed /g of dry biomass

300

Figure 1 Metal uptake, expressed as milligram of metal removed per gram of biomass dry weight, of Rhodopseudomonas palustris strains 42OL, SC0, AV32a, AV33, CGA009, Rhodobacter sphaeroides strain AV1, Cyanothece sp. strains 16Som2, CE4, VI22, and Nostoc PCC7936, in monometal solutions of Au, Cu, Ni or Zn. Data are mean values of five independent experiments, bars represent standard deviation. ( ) Au; ( ) Cu; ( ) Ni and ( ) Zn.

■

□

240 220 200 180 160 140 120 100 80 40 20

□

Figure 2 Metal uptake, expressed as milligram of metal removed per gram of biomass dry weight, of strains Cyanothece 16Som2, Cyanothece CE4 and Cyanothece VI22 utilized, without any acid pretreatment, in an Au-containing industrial wastewater. Data are mean values of five independent experiments, bars represent standard deviation. ( ) Au; ( ) Cu; ( ) Ni and ( ) Zn.

260

60

0 AV32

mg of metal removed per g dry biomass

■

280

AV33 AV1CPC42OL

SC0

CGA00 Nostoc VI22

CE4

16SOM2

220 200 180 160 140 120 100 80 60 40 20 0 16Som2

Cyanothece 16Som2, VI22 and CE4, respectively. Cu and Ni were removed at very low q values, never exceeding 3–4 mg g1. In the experiments carried out with the acid-pretreated biomass (Fig. 3), a significant decrease in the q values towards Au was observed. Indeed, the q values observed were 82 ± 7, 37 ± 13 and 35 ± 5 mg g1, for Cyanothece 16Som2, CE4 and VI22, respectively, while Ni was removed only by Cyanothece 16Som2 and CE4, at q values of 49 ± 15 and 10 ± 7, respectively. The two other metals were removed at very low q values, never exceeding 2 mg g1. Tests for the scaling up of the Au bioremoval process on industrial wastewaters The tests were carried out using 1 or 8 l of biomass suspensions of Cyanothece 16Som2, the strain that in the

CE4

VI22

earlier reported laboratory experiments showed the best Au bioremoval on the industrial wastewaters. In test L1, 8 l of biomass suspension was used without any pretreatment while in the two other tests the biomass was used after having been concentrated from 8 to 1 l by evaporation at 40°C (test L2) or at 100°C (test L3). The best q value towards Au was observed in test L3, with a value of 60 ± 3 mg g1, but at the same time the biomass removed Ni at a q value of 64 ± 4 mg g1, while Cu and Zn were not removed at all from the wastewater (Fig. 4). In the two other tests, Au was removed at q values of 32 ± 1 and 39 ± 2 mg g1 (tests L1 and L2, respectively) while, among the other metals, only Ni in test L1 was found to be removed with a q value of 64 ± 4 mg g1 (Fig. 4). In the case of the two other metals, null or negligible removal was observed in all the tests. After the contact with the Au-containing wastewater, the cyanobacterial biomass was incinerated and the


1383

mg of metal removed per g dry biomass


G. Colica et al.

90 80 70 60 50 40 30 20 10 0 16Som2 P

CE4 P

VI22 P

Figure 3 Metal uptake, expressed as milligram of metal removed per gram of biomass dry weight, of strains Cyanothece 16Som2, Cyanothece CE4 and Cyanothece VI22 utilized, after an acid pretreatment with 03% HCl for 6 h, in an Au-containing industrial wastewater. Data are mean values of five independent experiments, bars represent standard deviation. ( ) Au; ( ) Cu; ( ) Ni and ( ) Zn.

■

□

80 70 60

mg g–1

50 40 30 20 10 0 Au(L1) Cu(L1) Ni(L1) Zn(L1) Au(L2) Cu(L2) Ni(L2) Zn(L2) Au(L3) Cu(L3) Ni(L3) Zn(L3)

ashes obtained were analysed by electronic scansion microscopy (SEM) provided with EDAX-EDS integrated system (Fig. 5). The ashes obtained from the biomass used in test L1 showed a content of 6 mg Au (g ashes)1, while those obtained at the end of tests L2 and L3 showed an Au content of 24 and 36 mg g1, respectively. Discussion The capability of EPS-producing cyanobacteria to remove heavy metals from water solutions is well known (De Philippis et al. 2011), but only a limited number of studies is available on the use of cyanobacteria for the biosorption of Au from water solutions (Das 2010; Syed 2012). On the other hand, PNSB have previously shown good sorption properties towards Cd, Pb, Ru and also towards Au (Seki et al. 1998; Feng et al. 2007, 2008; Bai et al. 2008; Colica et al. 2012). In the screening carried 1384

Figure 4 Metal uptake, expressed as milligram of metal removed per gram of biomass dry weight, of Cyanothece strain 16Som2 utilized in Au-containing industrial wastewater. Columns represent the removal of the various metals in experiments carried out with the biomass utilized as it is (L1), after a concentration at 40°C (L2) or at 100°C (L3). Data are mean values of five independent experiments and bars represent standard deviation.

out in this study with four cyanobacteria e six PNSB, only the cyanobacteria showed high Au uptake performances. In particular, the q value of 318 mg g1 (equivalent to 16 mmol g1) obtained with Cyanothece CE4 with pure Au solutions is among the highest so far reported for cyanobacteria and for other micro-organisms and macroalgae (Kuyucak and Volesky 1989; Chakraborty et al. 2008; Cui and Zhang 2008; Song et al. 2008; Das 2010). The PNSB tested showed much lower Au sorption performances in comparison with EPS-producing cyanobacteria. In any case, three of them showed higher q values than the only other PNSB tested at comparable Au concentration (Feng et al. 2007). The strong anionic character of the polysaccharidic external layers of the cyanobacteria tested (De Philippis et al. 1998, 2000) most probably favoured the sorption of the positively charged Au ions in comparison with PNSB, which are devoid of such high number of negative binding sites.


G. Colica et al.


(b)

(a)

Mag HV Pressure Spot Tilt Det WD 300x 25·0 kV 1·00 Torr 5·0 0·3 ° LFD 12·5 mm

300·0µm

polisac bol tost

(d)


(c)


300·0µm

polisac bol tost

(e)

300·0 µm

tq cell


300·0µm

polisac rt A+B

(f)

WD Mag HV Pressure Spot Tilt Det 300x 25·0 kV 1·00 Torr 5·0 0·3 ° LFD 10·0 mm

300·0µm

tq polisac


300·0µm

polisac rt tost

Figure 5 SEM microphotographs of the ashes obtained by incineration of the cyanobacterial biomass recovered at the end of the wastewater treating process. The clear zones are due to the gold present on the surface of the ashes. (a, b) Ashes obtained from test L1; (c, d) ashes obtained from test L2; (e, f) ashes obtained from test L3.

All the cyanobacterial strains tested in single metal solutions also showed the capability to remove Cu, in some cases at high q values, a property that is rather undesirable if the biosorbent is intended to be used for the selective removal and recovery of gold. However, this picture completely changed when the three cyanobacterial strains that showed the best performances in pure metal solutions were tested using a real Au-containing industrial wastewater. In this case, the q value towards Au of strain Cyanothece CE4 dramatically decreased to a value 16% of that observed in single metal solution, while the q values of Cyanothece strains 16Som2 and VI22 remained almost the same as in pure solutions. It is most probable that the significant differences observed in the chemical features of the polymers constituting the exocellular polysaccharidic layers of the three cyanobacteria have determined a different interaction with the other metals and chemical compounds present in the wastewater, significantly affecting their capability to bind Au. Indeed, the polymer synthesized by Cyanothece CE4 is characterized by a very high content of uronic acids (801% on total carbohydrates) in comparison with a content of 408 and 206% reported for the polymers synthesized by Cyanothece VI22 and 16Som2, respectively (De Philippis et al.

1998). The high content of negative charges on the EPS may have favoured the interference with Au adsorption of positively charged metal ions, particularly in the case of Ni that is present in the wastewater at a very high concentration. Moreover, the different content of hydrophobic constituents (i.e. deoxysugars and acetyl groups) in the three EPSs (De Philippis et al. 1998) may have caused significant differences in their interaction with the organic additives present in the wastewaters of the Au plating process. Actually, a drastic change in the biosorption properties of microbial biosorbents used in pure metal solutions or in real wastewaters was already described for other microbial biosorption processes (Colica et al. 2010, 2012). However, in the real wastewater, the removal of Cu by the three cyanobacterial strains became negligible, probably owing to the relatively low concentration of this metal in the wastewater, two orders of magnitude lower than the concentration of Au and Ni. On the other side, the removal of Ni was comparable with, or even higher than, that of Au being the two metals present in the wastewater at a comparable concentration. Indeed, the Ni specific uptake shown by the three cyanobacteria significantly increased from values in the range 18–58 mg g1, for single metal solutions, to values


1385


G. Colica et al.

ranging between 90 and 214 mg g1 with the industrial wastewater. An explanation of this phenomenon could reside in the presence, in the wastewater, of comparable concentrations of Au and Ni. Another possible explanation is the presence in the wastewater of compounds capable of facilitating the accession of Ni ions to the binding sites on the biomass, as it was previously reported for similar kind of experiments (Gadd 2009). The three cyanobacterial strains that showed the best performances on pure metal solutions were used for Au removal from wastewaters with and without an acid pretreatment. The acid pretreatment is generally carried out to improve the biosorption performances by increasing the number of binding sites easily available for metal cations (Paperi et al. 2006). However, in the case of the previously described experiments, the pretreatment caused a decrease in the metal removal capability of the three cyanobacteria. This phenomenon might be related with the characteristics of the binding sites specific for Au. Indeed, in multimetal solutions, three different kinds of interactions between the metals have been observed: neutral, antagonistic and synergistic interactions (Micheletti et al. 2008a). Among these possible interactions, a synergistic effect takes place when the presence of specific metal ions on the exocellular polysaccharidic layers facilitates the binding process of the ions of another metal by enhancing the accessibility and increasing the availability of binding sites for the ions of this metal (Chen and Yang 2005; Micheletti et al. 2008a). In the previously described experiments, the acid pretreatment might have removed metal ions, bound to the polysaccharidic external layers that are essential for a high binding activity of the sites specific for Au (Micheletti et al. 2008a). The tests carried out for defining the procedures for the scaling up of the process were primarily addressed to investigate the best treatment of the biomass for its use in an industrial process. In particular, the use of concentrated biomass for designing plants of small dimensions was assessed. The best q value towards Au (60 mg g1) was obtained with Cyanothece 16Som2 biomass concentrated at 100°C. This value, equivalent to 0304 mmol of Au sorbed per g of cell dry weight, is comparable with the best values of biosorbents reported in the literature, which range between 0360 and 0218 mmol g1, respectively, obtained with Erwinia herbicola and Arthobacter tumescens in pure Au solutions (Tsuruta 2004). The data so far reported for cyanobacteria are much lower, ranging from 0026 mmol g1, shown by Spirulina platensis (Savvaidis 1998), to 0017 and 0010 mmol g1, respectively, shown by Rhizoclonium hieroglyphicum and Lyngbia majuscola (Chakraborty et al. 2008). However, the biomass 1386

concentrated at 100°C also showed a high q value towards Ni, thus reducing the interest in exploiting this treatment for the subsequent recovery of Au from the cyanobacterial biomass. For this purpose, it seems more advisable the use of the biomass concentrated at 40°C, which showed a lower q value towards Au than the biomass concentrated at 100°C but without showing any biosorption of the other metals. This biomass also showed a 33% lower amount of Au recovered from the incinerated biomass in comparison with the biomass concentrated at 100°C. However, it is worth stressing that, evaluating the whole process, the lower efficiency in the Au biosorption shown by the biomass concentrated at 40°C is positively counterbalanced by the advantage deriving from the elimination of the need to remove Ni from the Au recovered. In conclusion, this study showed the good potential of some EPS-producing cyanobacteria for the recovery of Au from the waste waters of plating industries but also pointed out the need to further investigate the correlations between the chemical features of the EPSs, and their capability to interact with Au in wastewaters and to design an efficient technology for recovering the metal from the biomass. References Anon. (2009) World Gold Council: Gold Bullettin, 42, No 3. Bai, H.J., Zhang, Z.M., Yang, G.E. and Li, B.Z. (2008) Bioremediation of cadmium by growing Rhodobacter sphaeroides: kinetic characteristic and mechanism studies. Bioresour Technol 99, 7716–7722. Bianchi, L., Mannelli, F., Viti, C., Adessi, A. and De Philippis, R. (2010) Hydrogen-producing purple non sulfur bacteria isolated from the trophic lake Averno (Naples, Italy). Int J Hydrogen Energy 35, 12216–12223. Chakraborty, N., Banerjee, A., Lahiri, S., Panda, A., Ghosh, A. N. and Pal, R. (2008) Biorecovery of gold using cyanobacteria and an eukaryotic alga with special reference to nanogold formation – a novel phenomenon. J Appl Phycol 21, 145–152. Chen, J.P. and Yang, L. (2005) Chemical modification of Sargassum sp. for prevention of organic leaching and enhancement of uptake during metal biosorption. Ind Eng Chem Res 44, 9931–9942. Chong, H.K. and Volesky, B. (1995) Description of two-metal biosorption equilibria by Langmuir-type models. Biotechnol Bioeng 47, 451–460. Colica, G., Mecarozzi, P.C. and De Philippis, R. (2010) Treatment of Cr(VI)-containing wastewaters with exopolysaccharide-producing cyanobacteria in pilot flow through and batch systems. Appl Microbiol Biotechnol 8, 1953–1961.


G. Colica et al.

Colica, G., Caparrotta, S. and De Philippis, R. (2012) Selective biosorption and recovery of Ruthenium from industrial effluents with Rhodopseudomonas palustris strains. Appl Microbiol Biotechnol 95, 381–387. Crist, H.R., Oberholser, K., Shank, N. and Nguyen, M. (1981) Nature of bonding between metallic ions and algal cell walls. Environ Sci Technol 15, 1212–1217. Cui, J. and Zhang, L. (2008) Metallurgical recovery of metals from electronic waste: a review. J Hazard Mater 158, 228–256. Darnall, W.D., Greene, B., Henzel, M.T., Hosea, M.J., McPerson, A.R., Sneddon, J. and Alexander, D.M. (1986) Selection recovery of gold and other metal ions from an algal biomass. Environ Sci Technol 20, 206–208. Das, N. (2010) Recovery of precious metals through biosorption – a review. Hydrometallurgy 103, 180–189. De Philippis, R., Margheri, M.C., Pelosi, E. and Ventura, S. (1993) Exopolysaccharide production by a unicellular cyanobacterium isolated from a hypersaline habitat. J Appl Phycol 5, 387–394. De Philippis, R., Margheri, M.C., Materassi, R. and Vincenzini, M. (1998) Potential of unicellular cyanobacteria from saline environments as exopolysaccharide producers. Appl Environ Microbiol 64, 1130–1132. De Philippis, R., Faraloni, C., Margheri, M.C., Sili, C., Herdman, M. and Vincenzini, M. (2000) Morphological and biochemical characterization of the exocellular investments of polysaccharide-producing Nostoc strains from the Pasteur Culture Collection. World J Microbiol Biotechnol 16, 655–661. De Philippis, R., Paperi, R. and Sili, C. (2007) Heavy metal sorption by released polysaccharides and whole cultures of two exopolysaccharide-producing cyanobacteria. Biodegradation 18, 181–187. De Philippis, R., Colica, G. and Micheletti, E. (2011) Exopolysaccharide-producing cyanobacteria in heavy metal removal from water: molecular basis and practical applicability of the biosorption process. Appl Microbiol Biotechnol 92, 697–708. Feng, Y.Z., Yu, Y.C., Wang, Y.M. and Lin, X.G. (2007) Biosorption and bioreduction of trivalent Aurum by photosynthetic bacteria Rhodobacter capsulatus. Curr Microbiol 55, 402–408. Feng, Y.Z., Lin, X.G., Wang, Y.M., Wang, Y. and Hua, J.F. (2008) Diversity of Aurum bioreduction by Rhodobacter capsulatus. Mater Lett 62, 4209–4302. Gadd, G.M. (2009) Biosorption: critical review of scientific rationale, environmental importance and significance for pollution treatment. J Chem Technol Biotechnol 84, 13–28. Gadd, G.M. and White, C. (1993) Microbial treatment of metal pollution—a working biotechnology. Trends Biotechnol 11, 353–359.


Hammouda, O., Gaber, A. and Raouf-Abdel, N. (1995) Microalgae and wastewater treatment. Ecotoxicol Environ Saf 31, 205–210. Kuyucak, N. and Volesky, B. (1989) Accumulation of gold by algal biosorbent. Biorecovery 1, 189–204. Leao, V.A. and Ciminelli, V.S.T. (2000) Application of ion exchange resins in gold hydrometallurgy. A tool for cyanide recycling. Solvent Extr Ion Exch 18, 567–582. Lengke, M.F., Ravel, B., Fleet, M.E., Wanger, G., Gordon, R. A. and Southarn, G. (2006) Mechanisms of gold accumulation by filamentous cyanobacteria from gold (III)-chloride complex. Environ Sci Technol 40, 6304–6309. Lin, Z., Wu, J., Xue, R. and Yang, Y. (2005) Spectroscopic characterization of Au3+ biosorption by waste biomass of Saccharomyces cerevisiae. Spectrochim Acta 61, 761–765. Mack, C., Wilhelmi, B., Duncan, J.R. and Burgess, J.E. (2007) Biosorption of precious metals. Biotechnol Adv 25, 264–271. Mata, Y.N., Torres, E., Bla´zquez, M.L., Ballester, A., Gonza´lez, F. and Mun˜oz, J.A. (2008) Gold (III) biosorption and bioreduction with the brown alga Fucus vesiculosus. J Hazard Mater 166, 612–618. Micheletti, E., Colica, G., Viti, C., Tamagnini, P. and De Philippis, R. (2008a) Selectivity in the heavy metal removal by exopolysaccharide-producing cyanobacteria. J Appl Microbiol 105, 88–94. Micheletti, E., Pereira, S., Mannelli, F., Moradas-Ferreira, P., Tamagnini, P. and De Philippis, R. (2008b) Sheathless mutant of cyanobacterium Gloeothece sp strain PCC 6909 with increased capacity to remove copper ions from aqueous solutions. Appl Environ Microbiol 74, 2797–2804. Niu, H. and Volesky, B. (2000) Gold-cyanide biosorption with L-cysteine. J Chem Technol Biotechnol 75, 436–442. Paperi, R., Micheletti, E. and De Philippis, R. (2006) Optimization of copper sorbing-desorbing cycles with confined cultures of the exopolysaccharide producing cyanobacterium Cyanospira capsulata. J Appl Microbiol 101, 1351–1356. Rhee, K.I., Lee, J.C., Lee, C.K., Joo, K.H., Yoon, J.K., Kang, H. R., Kim, Y.S. and Sohn, H.J. (1995) A recovery of gold from electronic scrap by mechanical separation, acid leaching and electrowinning. In Recycling Metals and Engineered Materials ed. Queneau, P.B. and Peterson, R.D. pp. 469–478. Pennsylvania: The Minerals, Metals & Materials Society. Savvaidis, I. (1998) Recovery of gold from thiourea solutions using micro-organisms. Biometals 11, 145–151. Seki, H., Suzuki, A. and Mitsueda, S.I. (1998) Biosorption of heavy metal ions on Rhodobacter sphaeroides and Alcaligenes eutrophus H16. J Colloid Interface Sci 197, 185–190.


1387


G. Colica et al.

Song, H.P., Li, X.G., Sun, J.S., Xu, S.M. and Han, X. (2008) Application of a magnetotactic bacterium, Stenotrophomonas sp. to the removal of Au (III) from contaminated wastewater with a magnetic separator. Chemosphere 72, 616–621. Syed, S. (2012) Recovery of gold from secondary sources – a review. Hydrometallurgy 115, 30–51. Ting, Y.P., Lawson, F. and Prince, I.G. (1991) Uptake of cadmium and zinc by the alga Chlorella vulgaris: part II. Multi-ion situation. Biotechnol Bioeng 37, 445–455.

1388

Tsuruta, T. (2004) Biosorption and recycling of gold using various micro-organisms. J Gen Appl Microbiol 50, 221–228. Volesky, B. (2003) Sorption and Biosorption. pp. 320. Montreal, Canada: BV Sorbex Inc. Volesky, B. and May-Phillips, H.A. (1995) Biosorption of heavy metals by Saccharomyces cerevisiae. Appl Microbiol Biotechnol 42, 797–806.
