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Received: 9 March 2010 Revised: 17 April 2010 Accepted: 1 May 2010 Published online in Wiley Online Library: 16 June 2010
Abstract
BACKGROUND: Yeast cells have been recognized as an effective type of biomass for the treatment of wastewaters containing
heavy metals. However, its capability to treat efficiently complex effluents loaded with several metals ions (Cr, Cu, Ni and Zn)
has never been reported. The aim of this work was to study the feasibility of a hybrid technology, which combines chemical
precipitation at pH 6.0 with a subsequent biotechnological-based process (using heat-killed cells of a flocculent brewing strain
of Saccharomyces cerevisiae), to remove simultaneously several metals from real electroplating effluents.
RESULTS: Two effluents containing Cu, Ni and Zn (effluent A) or Cr, Cu and Ni (effluent B) were treated. In both effluents, pH was
adjusted to 6.0; in effluent B, Cr(VI) was previously reduced to Cr(III). Chemical speciation studies allowed defining the amount
of biomass to be employed with a minimum number of batches. Subsequently to pH adjustment to 6.0, effluents were fully
treated with a serial batch of biomass. After the third batch, metal concentrations were lowered to below the legal limits of
discharge; removals ≥ 89, 91, 92 and 94% were attained for Ni, Cu, Cr and Zn, respectively.
CONCLUSIONS: In the present work, the usefulness of using flocculent brewing yeast cells to treat complex industrial effluents
loaded with several heavy metals was demonstrated. The hybrid process developed was shown to be an efficient alternative for
the treatment of real electroplating effluents.
c 2010 Society of Chemical Industry
Keywords: biosorption; chemical speciation; electroplating wastewater; heavy metals bioremediation; flocculent yeast
Among the different types of biological materials, Saccha- water. Cells were heat-inactivated by drying live cells, at 45 ◦ C, until
romyces cerevisiae has been recognized as an effective biomass for constant weight. In a previous work, it was found that cells were
the treatment of hazardous wastes containing heavy metals, as was dead after this treatment.13 After being heat-killed, cells were
reviewed by Wang and Chen.5 In particular, flocculent cells of S. washed five times with an excess of deionized water.
cerevisiae (flocculation is a characteristic usually found in brewing
yeast)6 can constitute a reliable supply of biomass for large-scale Determination of biomass
application in bioremediation processes. In this respect, it is well Cell concentration was determined spectrophotometrically (Uni-
documented that S. cerevisiae cells have the ability to remove Ag, cam, Helios γ ) at 600 nm after appropriate dilution of the samples
Mn, Cd, Co, Cr, Cs, Cu, Ni, Pb, Sr, U and Zn from water solution.7 – 14 in EDTA solution (30 mmol L−1 ) to prevent cell aggregation. Cal-
S. cerevisiae has the ‘status’ of ‘generally being recognized as safe’ ibration curves (absorbance versus either number of cells or dry
by the US Food and Drug Administration (FDA), which means that weight) were previously made.
it can be handled by humans without any concern. As a waste
product of brewing industries, this biomass can be obtained in Effluents characterization
large quantities at very low cost; these are two critical points Two effluents (A and B) from an electroplating industry of the
(availability and price), which should be taken into account when Metropolitan Area of Oporto, Portugal, were used in this study.
seeking a biomass for a biosorption-based technology.15 To characterize these effluents, pH value, redox potential, heavy
The accumulation of heavy metals by yeast cells is essentially metals (Cu2+ , Ni2+ , Zn2+ , total Cr and Cr6+ ), total inorganic ligands
a two-step process. The first step (initial biosorption) is rapid, (chlorides, sulphates, inorganic phosphates, nitrates and fluorides)
occurs in live and dead cells and is attributed to the interactions of and total organic and inorganic carbon concentrations were
yeast cell surface with the metals. The second (bioaccumulation) determined. Cr(VI) and inorganic ligands were analysed according
is a slower metabolism-dependent step, which occurs only in live to the Standard Methods.18 All determinations were done at least
cells.16 The accumulation of heavy metals by inactivated yeast in duplicate.
cells (bisosorption) is influenced by several factors such as the The determination of pH was attained with a conventional glass
presence of other cations and anions in solution. In addition, pH electrode using a pH meter Orion, model 4210.
and the presence of organic or inorganic ligands can affect metals Measurements of redox potential were performed using a
speciation (the different physicochemical forms of the metal in combined platinum-ring electrode (Metrohm).
solution, which together make up its total concentration)17 and In effluent A, fluorides were determined by direct potentiometry
consequently the available metal to be removed by yeast cells. using a fluoride-ion-selective electrode (Orion 96-09, Boston, USA)
This work reports the use of a hybrid technology for the assembled to a Kent 7045 pH meter. In the case of effluent B, due
treatment of two electroplating effluents in a batch mode. to the high amount of Cr and other heavy metals, which act as
The process developed combines chemical precipitation with interference, fluorides were determined by ion chromatography.
a subsequent biotechnological-based process (heat-treated cells For this purpose, the effluent was pretreated with an excess
of a flocculent brewer’s yeast of S. cerevisiae). In addition, a of sodium bisulphite to reduce Cr(VI) to Cr(III) and then, a
chemical speciation approach was used to define rationally the strong complexing agent (1,2 -cyclohexanedinitrilotetraacetic
amount of biomass to be applied for the efficient treatment of the acid) (CDTA) (Fluka) was added; the solution was heated at 60 ◦ C,
effluents with a minimum number of batches. The advantages of for 10 min. Afterwards, effluent was filtrated through a 0.45 µm
using a flocculent S. cerevisiae-based biosorbent for obtaining an pore size membrane and appropriately diluted. The samples were
effective, competitive and low-cost technology for the treatment injected into a mobile phase of sodium carbonate 0.9 mol L−1
of wastewaters loaded with heavy metals is discussed. (bubbled in nitrogen at 2000 psi) and carried through an ion
exchange column (Dionex AS9-HC), flowing at 1 mL min−1 , in an
ion chromatograph (Dionex DX-120).
MATERIAL AND METHODS Chlorides were determined by direct potentiometry using a
Strain, media and culture conditions
silver-ion electrode (Crison, Barcelona, Spain) assembled to a
In this work, the flocculent brewing strain of Saccharomyces Crison Basic 20 pH meter. This method can be used without a
cerevisiae National Collection of Yeast Culture (NCYC) 1364 was pretreatment step for samples containing phosphates, Cr and
used. The strain was routinely maintained at 4 ◦ C on YEPD agar other heavy metal ions. Barium nitrate and bisulphite buffer
slants (10 g L−1 yeast extract, 20 g L−1 peptone, 20 g L−1 glucose 0.4 mol L−1 , at pH 2, were added. The solution was titrated with a
and 20 g L−1 agar). standard AgNO3 solution.
Pre-cultures were prepared in 40 mL of YEPD broth (3 g L−1 Nitrates were determined by direct potentiometry using a
yeast extract, 5 g L−1 peptone and 20 g L−1 glucose) in 100 mL nitrate-ion-selective electrode (Crison, Barcelona, Spain) assem-
Erlenmeyer flasks. Cells were incubated at 25 ◦ C on an orbital bled to a Crison MicropH 2002 pH meter. The presence of
shaker Sanyo Gallenkamp IOC 400 (West Sussex, UK), at 150 rpm interfering chemical species (such as chlorides, nitrites, bicar-
for 24 h. bonate and complex organic acids), fluctuation of pH and ionic
Cultures in YEPD broth with 50 g L−1 glucose were prepared strength, were minimized by adding a buffer solution containing
by inoculating 1 L of culture medium in 2 L Erlenmeyer flasks silver sulphate, sulfamic and boric acid, at pH 3.0.
with 4% (v/v) from pre-cultures. Cells were incubated in the same Sulphates were determined using the turbidimetric method
conditions of the pre-culture for 48 h. with BaCl2 . To minimize the interference of suspended matter,
effluents were filtered through a 0.45 µm pore size membrane.
Preparation of cell suspensions Colour and turbidity due to the matter <0.45 µm were also
After growth, cells were harvested by centrifugation (2000g, 5 min) corrected by preparing effluent blanks without BaCl2 . In the case
and washed two times with 30 mmol L−1 ethylenediaminete- of effluent B, a standard addition method was used to minimize
1354
traacetic acid (EDTA) solution (Merck) and two times with deionized matrix interference.
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Removal of heavy metals using a brewer’s yeast strain of S. cerevisiae www.soci.org
standard deviation were not shown for pictorial clarity. for those metals having concentrations in the effluents above
Table 1. Physicochemical parameters of the raw electroplating effluents and after alkaline treatment (pH adjustment to 6.0)
The level of contaminants is compared to the US-Environmental Protection Agency (US-EPA)21 and the Portuguese22 wastewater limit discharge
criteria.
TC: total carbon. TOC: total organic carbon. IC: inorganic carbon.
a
After Cr (VI) reduction with bisulphide, dilution (four times) and pH adjustment to 6.0.
the limits of discharge, the theoretical amounts of metal ions and Fig. 2, respectively; theoretical simulation of cumulative
accumulated by yeast cells were chemically simulated using an percentages of metals removals (only for those metals, having
iterative process. For this purpose, the MINEQL+ software19 was concentrations in the effluents at pH 6.0 above the limits of
used. The program was run with a fixed concentration of biomass discharge) were also calculated and included in the figure.
up to 18 g L−1 , at pH 6.0, assuming the chemical composition of the Figure 2 shows that after the first batch, the highest removal
effluents (Table 1). Chemical simulations have shown that 18 g L−1 percentages were obtained for Cu (93% for both effluents);
of biomass should be efficient for the treatment of effluents A and thus, Cu concentration meets the quality criteria according to
B (diluted four times) at pH 6.0. Figure 1 shows species distribution the US-EPA and Portuguese law for both effluents. For effluent
of metals in solution (free metal ions plus metal ions complexed A, Ni and Zn removals were 57 and 59%, respectively; in the
with sulphates) and adsorbed to yeast cells, after the first batch, case of effluent B, Cr and Ni removals were 67 and 59%,
when 18 g L−1 of biomass is simulated. Cr, in effluent A, and respectively. In the subsequent batch, metal concentrations in
Cu and Zn, in effluent B, were considered in the theoretical solution were reduced and Cr concentration, in effluent B, reached
simulations, but not shown in Fig. 1, because concentration values the quality criteria, according to both laws. After the third batch,
in the effluents, at pH 6.0, were close to or below the discharge both effluents had metals concentrations in solution meeting
limits (Table 1). These simulations predict that the major amount of the quality criteria according to US-EPA and Portuguese law.
metals (>89%) should be removed (accumulated by the yeast cells) Ni and Zn concentrations, in effluent A, lowered to 2.4 and
after the first batch. Taking into account the chemical simulation 1.1 mg L−1 , respectively (Table 2). These values corresponded to
obtained above, the biotechnological-based treatments of both Ni and Zn cumulative removals of 89 and 94%, respectively,
industrial effluents, after chemical precipitation, were carried out which are in good agreement with the theoretical simulations
using 18 g L−1 of biomass; under these conditions, the molar ratio (Fig. 2). For effluent B, a similar behaviour was observed; total
[Biomass]/ [M] was 10 for both effluents. concentrations of Cr and Ni decreased to 1.2 and 2.2 mg L−1 ,
After chemical treatment (pH adjustment to 6.0), a serial batch after the third batch (Table 2). These values corresponded to
reactor, using new biomass in each batch, was implemented. total Cr and Ni cumulative removals of 92 and 90%, respectively,
Metal final concentrations and cumulative percentages of metal and are also in good agreement with the theoretical predictions
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removals obtained, after each batch, are present in Table 2 (Fig. 2).
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c 2010 Society of Chemical Industry J Chem Technol Biotechnol 2010; 85: 1353–1360
Removal of heavy metals using a brewer’s yeast strain of S. cerevisiae www.soci.org
(Table 1). This is due to the fact that the concentration of a soluble
60
metal ion in equilibrium with the corresponding insoluble metal
50 hydroxide, M(OH)x , at a fixed pH value is a constant value: [Mx+ (aq.) ]
40
= Kps/[OH− (aq.) ]x ; Kps is the solubility product and is a constant
value and the concentration of hydroxide, at a fixed pH value, is
30 also a constant value. Owing to the high insolubility of Cr(III) and
20 Cu hydroxides,20 this first step of effluents remediation (alkaline
treatment) allows the reduction in concentrations of Cr(III) and/or
10 Cu from real effluents to very low concentrations whatever the
0 initial concentration of these two metals in the wastewaters.
Ni Cr As can be seen in Table 1, after the alkaline treatment, effluents
Metal are suitable for implementing the biotechnological-based step.
This aspect is particularly important when we have multi-elements
Figure 1. Chemical simulation of the influence of biomass on the metal in the effluent competing for biomass, which frequently occurs
species distribution after the first batch. 18 g L−1 dry weight yeast cells
of S. cerevisiae were used. A – industrial effluent A; B – industrial effluent
in electroplating effluents. In fact, heavy metals removal by yeast
B. Metals associated with inactivated yeast cells (dashed bar); metals cells is pH dependent. At pH 2.0, metal cations uptake by yeast
associated with sulphate (black bar); free metal ions (white bar). Chemical cells is practically not observable, increasing with increasing pH,
simulations were performed with a chemical equilibrium computer and usually performed at pH values between 5 and 6.8,30,31
program (MINEQL+). In the present work, brewing flocculent yeast cells were used in
the biotechnological-based step. Yeast flocculation is a reversible
process wherein the individual cells aggregate into multicellular
DISCUSSION masses, called flocs (composed of thousands or even millions of
In recent years, different types of biomass (such as Sargassum cells), which sediment rapidly in the medium in which they are
wightii, Aspergillus niger, Aspergillus sydoni, Penicillium janthinellum, suspended.6 Flocculent yeasts have in their cell wall a specific
Ulva reticulata, Geobacillus thermodenitrificans) have been used lectin-like protein which allows interaction with the carbohydrate
for the treatment of wastewaters containing heavy metals.23 – 27 residues of the walls of neighbouring cells to establish a
However, the treatment of real effluents using S. cerevisiae has flocculent bond; in this process Ca2+ seems to ensure the correct
rarely been reported in the literature.28 The removal of heavy conformation of the lectins.6 Flocculent cells of S. cerevisiae have
metals is usually performed with a mono element in very simple a higher ability for Cu2+ accumulation than the non-flocculent
solutions, usually in almost total absence of anionic ligands.7,9,12,29 cells32 most likely due to the fact that heavy metals can also occupy
Real effluents are, as a rule, much more difficult to treat due lectin Ca2+ binding sites. In previous work, it was shown that yeast
to the presence of multi-metals and multi-ligands in solution. In cells, inactivated at 45 ◦ C, maintained their flocculent properties,
addition, the use of real effluents instead of synthetic (simulated) when compared with live cells, in industrial effluents and in a wide
ones constitutes a challenge in order to test and validate the range of synthetic effluents containing various metals. The yeast
efficacy of the use of microbial biomass in the bioremediation of strain used is able to form flocs of macroscopic size, achieving
heavy metals. a sedimentation >95% of cells within 5 min.12 In addition, killed
Heavy metals accumulation by dead yeast biomass can be yeast cells were able to accumulate higher quantities of Ni and Zn
due to one or more of the following mechanisms: adsorption, than live yeast cells, at pH 6.0.13 Since the removal of heavy metals
precipitation or complexation by yeast cell surface structure.16 and cell separation are simultaneously achieved when flocculent
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Most likely, carboxyl, amino, hydroxyl and amide groups of protein biomass is used, the employment of this type of cell looks to be
Table 2. Bioremediation of industrial effluents using S. cerevisiae NCYC 1364, in a batch mode reaction
The level of the metals reached is compared with the US-Environmental Protection Agency (US-EPA)21 and the Portuguese22 wastewater limit
discharge criteria.
ND: not determined; the metal concentrations were below the legal limit of discharge. NS: not specified in the law.
a Mean and standard deviation of three independent experiments performed in duplicate (n = 6).
b
Effluent A: after pH adjustment to 6.0. Effluent B: after Cr(VI) reduction with bisulphide, dilution (four times) and pH adjustment to 6.0.
a promising alternative for the bioremediation of metal-loaded 11 and 6%, respectively, whereas for effluent B, the differences
industrial effluents. Moreover, the natural aggregation properties for Ni and Cr were 10 and 8%, respectively. These differences
of flocculent yeast cells allows the use of the sedimentation tanks can be due to several factors: (i) overestimation of the values
already available in wastewater treatment plants of the major of metals adsorbed to yeast cells, calculated by the theoretical
electroplating industries for chemical precipitation of effluents. simulation, as a consequence of the stability constants between
The process can be feasibly engineered on a large scale and avoids these metals and inorganic ligands, used in the simulations, were
capital investment when changing from a conventional (chemical not determined in the experimental conditions of the effluents
precipitation) process to the process proposed. Moreover, a (e.g. ionic strength and temperature); (ii) the affinity constants
stirred batch tank reactor has the advantages of design simplicity, between metals and biomass8,13 were determined using the
stability of operation, and low operational and maintenance costs. Langmuir model; this model, which is most widely used, assumes
Together, these are important points when seeking a competitive that all sites of the biomass have the same affinity and does
and inexpensive technology. In addition, if desired, flocculent not include the heterogeneity of the yeast cells and the effects
yeast cells can also be used in continuous mode, in columns, of ionic strength and metal mixtures;33,34 (iii) complexation of
without the risk of biomass washout.12 metals by organic matter present in the real effluents and soluble
As can be seen in Table 2, after the first batch, the concentrations organic matter leached from the microorganisms; the release
of Cu were below the limits of discharge criteria21,22 in both of metal binding agents into solution from the cytoplasm of
effluents. This was due to the high insolubility of Cu hydroxide, yeast cells as a consequence of damage to the cell membrane
which allows the removal of a large amount of Cu from solution by during the drying process,13 complex metals and thus reduce the
chemical precipitation at pH 6.0. Additionally, the high affinity of efficiency of the bioremediation process.35,36 The values of TOC
yeast cells for Cu efficiently removes the remaining concentration in both effluents were ≤11 mg L−1 (Table 1), which indicates that
of Cu in solution. These results demonstrate that, for effluents effluents contain low amounts of organic matter. However, it is
containing only Cu, application of this hybrid technology at pH 6.0 important to point out that minor amounts of strong complexing
is efficient, after the first batch, whatever the initial concentration agents, such as ethylenediaminetetracetic (EDTA) or nitrilotriacetic
of Cu present in the effluent. acid (NTA) and citric acid can be present in the effluents as they
The percentage Cu removals found in experiments (93% for both are used in the soak cleaning and pickling steps,37 respectively.
effluents) are in very good agreement with theoretical simulations, These compounds complex strongly with these metal ions20 and
for which Cu removals of 97 and 98% were predicted for effluents A their presence, even in minor amounts, can raise the amount
and B, respectively (Fig. 2). On the other hand, the percentages of of soluble metal ions not available to be accumulated by yeast
experimental removals found for the other metals (Cr, Ni and Zn) in cells.
both effluents were lower than the theoretical simulations (Fig. 2). Heat-treated flocculent yeast cells have been shown to be very
However, the differences between theoretical and experimental effective for metals removal from industrial effluents. After the
values were attenuated with the number of cycles; after the third batch, both effluents were treated (Table 2), with removals of
1358
third cycle, for effluent A, the differences for Ni and Zn were Ni, Cu, Cr and Zn ≥ 89, 91, 92 and 94%, respectively. As was reported
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c 2010 Society of Chemical Industry J Chem Technol Biotechnol 2010; 85: 1353–1360
Removal of heavy metals using a brewer’s yeast strain of S. cerevisiae www.soci.org
A 100 CONCLUSIONS
In this work, a hybrid technology, combining chemical precipi-
80 tation with subsequent biosorption at pH 6.0 was developed for
Metal removal (%)
0 3rd
1 st
2nd ACKNOWLEDGEMENTS
The authors thank the Fundação para a Ciência e a Tecnologia (FCT)
Cu Cr Ni from the Portuguese Government for the financial support of this
Figure 2. Comparison of theoretical and experimental metals removal work with FEDER funds, under the Project POCTI/CTA/47875/2002.
from electroplating effluents by S. cerevisiae NCYC 1364 through a series Manuela D. Machado also acknowledges a grant scholarship
of sequential batches in bench scale experiments. A – industrial effluent financed under the same project and another grant from FCT
A; B – industrial effluent B. Theoretical values: white bar; experimental (SFRH/BD/31755/2006).
values: dark bar. Theoretical calculations were performed with a chemical
equilibrium computer program (MINEQL+), as described in the text.
Experimental assays were carried out with 18 g L−1 dry weight of biomass,
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c 2010 Society of Chemical Industry J Chem Technol Biotechnol 2010; 85: 1353–1360