Environment International 36 (2010) 299–307

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Environment International
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / e n v i n t

Review article

Biosorption and bioaccumulation – the prospects for practical applications

Katarzyna Chojnacka ⁎
Institute of Inorganic Technology and Mineral Fertilizers, Wrocław University of Technology, ul. Smoluchowskiego 25, 50-372 Wrocław, Poland

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

Article history: The paper summarizes the present and future course of biosorption and bioaccumulation, as the branch of
Received 20 August 2009 science, pointing out on their basic assumptions, philosophy and the goals. The processes are presented as new
Accepted 2 December 2009 tools for separation technologies of XXI century. The paper is the discussion with the literature on the future
Available online 6 January 2010
prospects of those processes, pointing out that research should be oriented on the practical applications, in order
to make technologies from the processes and also discusses other than environmental possible future
Keywords:
Biosorption
applications. It presents an own point of view on these techniques, after some years of working in this very area.
Bioaccumulation Biosorption and bioaccumulation, involve interactions and concentration of toxic metals or organic pollutants
Toxic metals (e.g. dyes) in the biomass, either living (bioaccumulation) or non-living (biosorption). The processes play an
Organic pollutants important role in natural cycling of matter in the environment. The paper discusses the possibilities which offer
Wastewater treatment research on pollutants-biomass interactions, pointing out that the key to elaborate an efficient method working
for the nature would be to understand the mechanisms governing the processes, parameters which influence
both equilibrium and kinetics, through the observation of naturally occurring phenomena. Only then we would
be able to control and carry out under industrial regime, so the processes would work beneficially for the
environment.
© 2009 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 299
2. Biosorption . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 301
3. Technology and commercial applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 303
4. Bioaccumulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 304
5. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 306
Acknowledgments. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 306
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 306

1. Introduction concentration, with a possible recovery and reuse (Volesky, 1997).

One of the main problems of the society in the XXI century is
environmental pollution. The main pollutants include toxic metals,
the quantity of which permanently increases in the environment as
the result of increased industrial activity which mines metals from
inert deposits underground. Once toxic metals are present in the
environment they undergo cycles between its abiotic and biotic
elements, posing toxicity in the latter group. Since it is impossible to
degrade those pollutants by any means, the only way to remove them
from the environment is to exclude metals from cycling through their
⁎ Tel.: + 48 71 320 43 25; fax: + 48 71 320 34 69.
E-mail address: katarzyna.chojnacka@pwr.wroc.pl.
This would also reduce the consumption of non-renewable resources
(Chojnacka, 2010).
The problem is of particular significance to human as the final
consumer, since on each level of the trophic chain biomagnification
occurs. If toxic metals become bioaccumulated by an organism of
human, several disadvantageous symptoms from eg. gastrointestinal,
neurological and immunological systems are observed. The mostly
dangerous metals include so-called ‘toxic trio’: cadmium, lead and
mercury, for which no biological function has been found, yet. But
there is a long list of other metals which although essential in low
doses, in high – become toxic, as well.
The law which regulates maximum acceptable concentrations of
toxic metals in wastewaters discharged into water and soil or drinking
waters became more restrictive, recently and at present accepts the

0160-4120/$ – see front matter © 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.envint.2009.12.001
300 K. Chojnacka / Environment International 36 (2010) 299–307
maximum permissible levels of a fraction of mg/l or µg/l (Chojnacka,
2010). Conventionally used methods became either expensive, not-
efficient or require the use of aggressive conditions if wastewater or
water are to be treated to such low concentrations (Schiewer and
Volesky, 2000). For this reason, there is the need to search for new
techniques, which would be suitable to be used as the final, polishing
step, and would be designed to remove pollutants to the level lower
which is required by law (Veglio and Beolchini, 1997). It would be also
advantageous for these methods to enable recovery and reuse of
metals.
Frequently, efficient and useful solutions can be found by the
observation of processes which naturally occur in the environment. If
soluble chemicals are present in aqueous environment, where also the
biomass can be found, sorbates interact with biological materials – are
bound to cellular surfaces in the process called biosorption or become
accumulated inside the cells via bioaccumulation (Chojnacka, 2010;
Kaduková and Virčíková, 2005). Biosorption and bioaccumulation
participate in the cycle of matter in the environment. Because living
organisms bioaccumulate chemical substances, pollutants become
toxicants, as well. The processes occur permanently and are
performed by virtually all types of the biomass. In natural environ-
ment human is not able to take control over these processes, although
they can find an application in the industrial practice under controlled
operation conditions. Biosorption and bioaccumulation also occur by
accident in virtually all biological wastewater treatment processes
and in all bioremediation technologies (Rehman et al., 2006). In some
cases, there are also process solutions which support the occurrence
and efficiency of those phenomena by eg. contact stabilization
wastewater treatment process, where there is a special contact tank
designed to promote biosorption by increasing the concentration of
cells. Because biological sludges accumulate sorbates, so far no
efficient methods of their utilization have been proposed (Naja and
Volesky, 2010). On the other hand, those bound pollutants have been
previously removed from wastewater (Klimenko et al., 2002).
Biosorption and bioaccumulation differ in that in the first process
pollutants are bound to the surface of cell wall and in the second, they
become also accumulated inside the cell (Table 1). Biosorption is a
simple physicochemical process resembling conventional adsorption
or ion exchange. The difference lies in the nature of sorbent which in
this case is the material of biological origin. Biosorption is metabol-
ically-passive process. Since in biosorption equilibrium is reached, it
can be shifted into either side: left in wastewater treatment or right if
sorbate is to be removed and recovered (Fig. 1). In bioaccumulation,
the process goes further. This means that the first stage is biosorption
and then subsequent stages occur, related with transport of pollutant
(mainly via energy-consuming active transport systems) into inside
of cells and eventually the concentration of cells increases. Thus, in
bioaccumulation more binding sites for the pollutant are available and
lower residual concentrations can be reached. But in order for the
Table 1
The comparison between biosorption and bioaccumulation process (Chojnacka, 2010).
Biosorption Bioaccumulation
Passive process Active process
Biomass is not alive Biomass is alive
Metals are bound with cellular Metals are bound with cellular surface
surface and interior
Adsorption Absorption
Reversible process Partially reversible process
Nutrients are not required Nutrients are required
Single-stage process Double-stage process
The rate is quick The rate is slow
Not controlled by metabolism Controlled by metabolism
No danger of toxic effect Danger of toxic effects caused by
contaminants
No cellular growth Cellular growth occurs
Intermediate equilibrium concentration Very low equilibrium concentration
of metal ions of metal ions
Fig. 1. Schematic diagram of biosorption.
process to occur, some conditions need to be fulfilled. Bioaccumula-
tion is the cultivation of an organism in the presence of pollutants
which are to be removed.
If biosorption and bioaccumulation are to be performed under
laboratory conditions, in the first stage the biomass should be
suspended in the solution containing a sorbate. After a couple of
hours the equilibrium would be reached and if pollutant-laden
biomass would be separated on this stage, biosorption was performed.
But if the solution contains nutrients and can serve as a minimum
growth medium for the organism, it begins to carry out its metabolic
processes and activate intracellular transport systems. However, if
heterotrophic organisms (bacteria or fungi) are intended to be used,
organic carbon source should be supplied to wastewater. This is a
severe limitation, because wastewaters which are to be treated by
bioaccumulation rarely contain beside sorbate, also organic carbon
source. This concerns wastewater from metallurgical industry.
Supplementation of organic source is not advantageous. A solution
to this problem could be the use of photosynthetic organisms: either
algae or aquatic plants (Kara, 2004; Prasanna et al., 2008; Rose et al.,
1996), nutritive requirements of which are rather small and they
require inorganic carbon source which could be carbon dioxide from
flue gases. However, some papers report that at higher level of
pollutants, algae activate systems which protect from excessive
accumulation, resulting in low bioaccumulation capacity. The process
is thus useful only at low load of pollutants. On the other hand, the
requirement for an organic carbon source is critical for bioaccumula-
tion, however biological wastewater treatment systems contain
growth nutrients and bioaccumulation occurs in municipal wastewa-
ter treatment plants.
In bioaccumulation it is possible to reach lower residual concen-
tration of sorbate because cells offer binding sites on the surface and
inside the cell. In bioaccumulation a part of the sorbate is transported
into inside of cell, releasing thus binding sites present on the surface,
so additional amount of sorbate can be bound there according to the
course of the equilibrium biosorption dependence. Also, the concen-
tration of the biomass eventually increases, which enables to bind
even more sorbate.
Bioaccumulating organisms should be selected among species
which are resistant to high loads of pollutants and do not have
mechanisms which protect from excessive accumulation inside the
cell (Deng and Wilson, 2001; Kocberber and Donmez, 2007). They
should have rather mechanism of intracellular binding, such as special
proteins rich in thiol groups- metallothioneins, phytochelatins, which
are synthesized as the response to the presence of toxic metal ions in
their living environment, and complex those pollutants, thus
excluding them from normal metabolic processes (Fig. 2).
 K. Chojnacka / Environment International 36 (2010) 299–307
Fig. 2. The mechanism of biosorption and bioaccumulation.
Biosorption is metabolically passive process and is performed by
material of biological origin, not by living biomass. Bioaccumulation is
metabolically active and is performed by living cells. While in
biosorption there is no danger of posing toxicity by sorbate to sorbent,
in bioaccumulation such danger exists. However, if the method is
intended to be used as the final polishing step, the concentration of
bound substances would be of a magnitude of few mg/l.
Biosorption and bioaccumulation are mainly used for the removal
of metal cations from the solutions. The history of research on
biomass-metal interactions is dated back to 1960's. At this time it was
found that although the biomass cannot destroy metals, it can change
their properties in sometimes amazing ways. The processes of
biological metal binding were found to be useful for biohydrome-
tallurgy and biogeochemistry. Ten years later the first description of
bioaccumulation as the method of wastewater treatment was
elaborated. It was reported that in the lagoon in the vicinity of lead
and zinc mining and milling works a dense mat-like growth of algae
was observed (Naja and Volesky, 2010). The algae accumulated metal
cations and eliminated other, competing organisms. The history of
biosorption as a regular branch of science began in 1990's. A large
contribution as made here by prof. Bohumil Volesky from McGill
University in Canada, who provided many theoretical basis of the
process and also made first attempts to commercialize it. Metal
cations sequestering properties of the biomass were described. The
biomass was able to concentrate metal ca. 1000 times. The process
was found to be selective and for this reason metal recovery was
found to be possible. The biomass used in the process could be any
abundant and cheap biological material.
At present the majority of original research papers on biosorption
concerns binding of metal cations, which results from the chemical
composition of cell wall. Sorbates of particular interest include for
biosorption Cu, Cd, Pb, Cr, Zn, Ni and for bioaccumulation Cd, Cu, Hg,
Pb, Cr, Zn. The papers on biosorption are written by representatives of
various branches of science: chemists, (micro)biologists and (pro-
cess)engineers. Each scientist has its own, different, but equally
valuable point of view, with the each aspect important if a technology
is to be elaborated.
The effluents which can be treated by both, biosorption or
bioaccumulation, include wastewaters from metallurgical industry,
rinse waters from electroplating, metal finishing and printed circuit
boards manufacturing, mining operations, leachates, surface and
ground waters. There is a long list of sorbates which can be removed
by biosorption and bioaccumulation: Al, Cd, Cr, Co, Cu, Au, Fe, Pb, Mn,
Hg, Mo, Ni, Pt, Se, Ag, U, V, Zn.
301
2. Biosorption
The concept of biosorption includes concentrating a sorbent in the
biomass. The biological material laden with sorbate is then regener-
ated and reused, and sorbate is recovered by eluent. It is important to
choose desorbing agent very carefully, so all sorbate would be
removed from the biomass by low volume of solution and that the
biosorbent would not be destroyed and would sustains its sorptive
properties, so it can be reused in the subsequent biosorption cycle.
The concentrate of sorbent can be then treated by conventional
methods which preferably enable recovery of metal, such as eg.
electrolysis (Fig. 1).
Biosorption is defined as the process of concentration of sorbate and
a prefix ‘bio’ means that the sorbent is of biological origin, a surface of
biological matrix. The advantages of the process include low operation
costs if low-cost sorbents are used, low quantity of sewage sludge
disposed, COD of wastewater does not increase. The process is simple in
operation and very similar to conventional adsorption or ion-exchange,
except that sorbent of biological origin is employed. Biosorbents are
selective and regenerable and a process is in particular highly effective
in the treatment of dilute effluents (Orhan et al., 2006; Norton et al.,
2004). The limitations include first of all a shorter life time of
biosorbents when compared with conventional sorbents (Gadd, 2009).
Biosorbents are renewable sorbents. Those are materials of
bacterial, fungal, plant or animal origin (Alluri et al., 2007; Asma
Saeed et al., 2005; Gupta et al., 2000; Ivo et al., 2001; Muraleedharan
et al., 1995; White and Gadd, 1995). Frequently the biomass which we
would not suspect to have biosorptive properties can efficiently
sequester metal ions from solutions (Kuyucak, 1997), eg. crushed egg
shells, bones, peat, cotton waste or rice husk (Aksu, 2005).
Biosorbents can be classified into low- and high-cost sorbents. The
first group includes the materials which can be collected directly from
the environment (eg. seaweeds) and waste or by products from
industry, eg. yeasts from fermentation processes winery or brewery
(Wang and Chen, 2006). The latter group includes the materials which
are specially propagated for biosorption purposes. They should have
very good biosorptive properties and should be easily regenerable.
The new biosorbents should be characterized in terms of their
sorptive properties. The effect of operation conditions (pH, temper-
ature, the concentration of sorbate and sorbent) on biosorptive
capacity (expressed in either mg/g or meq/g) is determined.
For a long time the mechanism of biosorption was unknown. Several
different processes were thought to contribute to what was observed as
biosorption: surface complexation and precipitation, physical adsorp-
tion or ion exchange. But only recently the dominating role of the latter
process was confirmed. Since the mechanism was found to be ion
exchange, protons compete with metal cations for the binding sites and
for this reason pH is the operation condition which influences the
process the mostly strong (Schiewer and Volesky, 2000). The other
factors important in biosorption include the type and the concentration
of the biomass, and the sorbate, the mode of biosorption – if it is carried
out is suspension or by immobilized biomass, the presence of other
cations and anions. pH determines protonation or deprotonation of
metal ions binding sites and thus influences the availability of the site to
the sorbate. By lowering pH it is also possible to release metal ions from
the binding site. This property is used for the recovery of metal cations
and regeneration of the biosorbent.
The effect of pH on biosorption of cationic dyes is similar as inorganic
cations, since the mechanism is similar – organic cations are also bound
to negatively charged functional groups exposed by cellular surfaces.
Within a given group of organisms, biosorption properties are
similar, because the chemical composition of cell wall is alike. Seaweeds
are presented as very good sorbents, because the cell wall of green and
brown algae contains alginate with its carboxyl and hydroxyl groups
(Davis et al., 2003; Vieira and Volesky, 2000). Worse sorptive properties
possess red algae which contain carrageen, exposing hydroxyl and
302 K. Chojnacka / Environment International 36 (2010) 299–307

sulfonate groups (Vieira and Volesky, 2000). The biomass of yeasts and
other fungi contains chitin and chitosan and thus amino, amido and
hydroxyl groups are found on the cellular surfaces. For this reason fungi
have a unique properties of binding both cations and anions to their cell
wall. Among the group of bacteria we can distinguish gram positive and
gram negative. Cell wall of gram negative bacteria contains peptidogly-
can and of gram positive also teichoic acids containing phosphoryl and
hydroxyl groups and thus the latter are better biosorbents. Also
chemicals isolated from the biomass are used as biosorbents. This
concerns chitin, chitosan or alginate.
Generally the process of biosorption can be described as biological
ion exchange with binding groups present on the surface of cell wall:
carboxyl, sulfonate, phosphoryl, amido, amino, imidazole (Volesky and
Schiewer, 2000). The groups have distinguishable pKa responsible for
the binding properties of a given group (Volesky, 2007). So, if searching
for new biosorbents, it is possible to use a simple and cheap technique of
potentiometric titration and to determine the type and the concentra-
tion of a given group (Chojnacka et al., 2005). Other techniques which
enable identification of biosorptive sites include spectroscopic techni-
ques: IR, Raman, Electron Dispersive Spectroscopy (EDS), X-ray
Photoelectron Spectroscopy (XPS), Electron Microscopy (Scanning,
Transmission), Nuclear Magnetic Resonance (NMR), X-ray Diffraction
Analysis (Tsezos et al., 1997). Also, affinity constants between a group
and a sorbate can be determined and this enables description of
selectivity of the biomass for different sorbates.
The factors which influence biosorption performance include the
type of the biomass (and resulting the composition of cell wall), pH,
temperature, presence of other competing ions (both cations and
anions) (Naja et al., 2010) (Table 2). Generally, increase of pH causes
deprotonation of metal ions binding sites exposed by cellular surfaces.
Decreasing pH causes competition between protons and positively
charged metal ions. However these rules concern only cations (Naja
et al., 2010). Since biosorption is reversible process, decreasing pH
would result in deprotonation. This property is used in regeneration of
biosorbents. Another explanation is that with increased pH, solubility
of complexes of metals decreases (Naja et al., 2010).
Description of mechanism of biosorption and factors affecting its
performance is important for the optimization of the operation
conditions for biosorption itself and also for the regeneration of the
biosorbent. Describing the effect of pH requires understanding of
solution chemistry (hydrolysis, complexation, redox reactions, pre-
cipitation) which is influenced by this factor, the presence of anions in
the solution (Esposito et al., 2001; Ofomaja and Ho, 2007). pH
determines the speciation and solubility of toxic metal ions and also
affects the properties of the biomass (Xu et al., 2006). pH influences the
magnitude of negative charge on the surface of the material, by either
protonation of deprotonation metal binding sites (Ofomaja and Ho,
2007). Binding sites are available to metal ions only in deprotonated
state (Ofomaja and Ho, 2007). Therefore, pH influences chemistry of
metals in the solution and electrical charge of biomaterials (Ofomaja
and Ho, 2007). At present, many papers discuss the effect of this factor
on biosorption performance (Naja et al., 2005a,b, 2006; Esposito et al.,
2001; Xu et al., 2006; Ofomaja and Ho, 2007; Navarro et al., 2008) by
eg. determination of zeta potential, electrostatic attraction and the
contribution of ion-exchange mechanisms (Xu et al., 2006).
Cation-exchange properties of the surfaces of biological materials
can be investigated by acid-base or metal based potentiometric titration
(Naja et al., 2005b). Cation-exchange capacity can be determined by
using Gran's method and Henderson-Hasselbach's equation. Recently, a
new technique – high resolution titration was implemented (Naja et al.,
2005a). The aim was to determine the total concentration of cation-
exchange sites present on the surface of cells of biosorbent material.
Cation-exchange capacity determined by potentiometric titration was
correlated with biosorption capacity evaluated in biosorption experi-
ments (Naja et al., 2005a; Chojnacka et al., 2005), which showed that on
the surface of cells of biosorbents there are present functional groups
and these surfaces can be described as polyelectrolytes, because of the
presence of amino, carboxyl, phosphate and sulfate groups (Naja et al.,
2005a; Chojnacka et al., 2005). This concept was implemented in the
investigation of cation-exchange capacities of various bacteria and fungi
(Naja et al., 2005a) as well as algae (Chojnacka et al., 2005). Titration
results showed that carboxylic, phosphate groups and sulfonate
(although in lower extent because of lower content in the biomass)
during biosorption of Pb by Rhizopus arrhizus participated in biosorption
of metal ions (Naja et al., 2005b). This binding was confirmed by the use
of microscopic and spectroscopic techniques (Naja et al., 2005b). The
mechanism of biosorption which was postulated by the authors
included adsorption and micro-precipitation (Naja et al., 2005b).
Metal-based titration of biosorbents was carried out with the use of
ion-selective electrode, in order to differentiate the energetic sites
which are capable of the reaction with metal cations at their low
concentrations (Naja et al., 2006). Titration technique enabled to
determine acidic dissociation constants and also metal affinity con-
stants. If pH was higher than pKa, the groups were deprotonated and
available for metal ions (Ofomaja and Ho, 2007). In the literature, pH-
sensitive models describing equilibrium of the process were evaluated.
Basing on these equations, it was possible to determine the concentra-
tion of metal binding sites and pKa, and the models were derived from
pH titrations (Schiewer and Patil, 2008; Chojnacka et al., 2005). Other
than potentiometric methods used in identification of binding sites are
spectroscopic techniques (Volesky, 2007): IR, Ramam, Electron Disper-
sive Spectroscopy (EDS), X-ray Photoelectron Spectroscopy (XPS),
Electron Microscopy (Scanning, Transmission), Nuclear Magnetic
Resonance (NMR), X-ray Diffraction Analysis.

Table 2
Some facts on biosorption.

The role of functional groups Participation of functional groups in biosorption depends on (Vieira and Volesky, 2000):
– The concentration and the type of the group in the biomass
– The accessibility of the group
– The chemical state of the site (eg. availability)
– The affinity between site and metal (binding strength)
The role of pH pH (Aksu, 2005; Volesky and Schiewer, 2000)
– Affects protonation (= availability) of metal ions binding sites and ionic state of the sorbate in the solution
– At low pH (high level of H+), anionic sites become protonated
– Metal cations can be eluted by acidic wash – regeneration, multiple reuse, better economy
Sorbates Inorganic sorbates:
– Almost all metals (not K+, Mg 2+)
– Most thoroughly investigated – key environmental pollutants of major toxicity: Pb, Cu, Hg, Cd, Cr, As, radionuclides (Co, Sr, U, Th)
– In solution sorbates are in cationic, exist as complexes (Cl-), range of oxidation states, hydroxylated depending on pH.
– Studies assume divalent cations – not always true!
Organic sorbates:
– Yeasts bind mainly cations, but sometimes anions, eg. Rhizopus arrhizus (fungus) coordinates U to amine of chitin with further
precipitation of hydroxylated derivatives (Vieira and Volesky, 2000).
 K. Chojnacka / Environment International 36 (2010) 299–307
Sorbates preferably removed by biosorption are metal cations, but
also anions can be removed by fungi. In some cases also organic
compounds, e.g. a reactive dye, Remazol Blue (Aksu and Dönmez, 2003),
are bound by the biomass in the process of biosorption. In this case,
biosorption can be used for decolorization of wastewaters (Aksu, 2005).
Among metal cations, virtually all ions are bound except alkali and
alkaline earth metal ions which are naturally bound with the functional
groups and are rather released from the biomass than bound.
In order to make the process useful in industrial practice, it is
necessary to propose a mathematical description. Always when modeling
processes performed by the biomass, several simplifications are required.
Also in the case of biosorption modeling, the equations are rather of
empirical than physical character. Kinetics of biosorption is usually
described with pseudo-first or pseudo-second order model and the
equilibrium more frequently with Langmuir than Freundlich equation,
because a clear plateau can be distinguished on the sorption isotherm.
The majority of biosorbents has finite number of sorption sites, so it is
possible to define the maximum biosorption capacity.
Biosorption is a quick process. The equilibrium is usually reached
within few minutes. Since the rate of the process is high, in some cases
it is even difficult to select and fit the proper equation and to
determine the order of the reaction due to errors related with quick
sampling. The process is usually described with either first-, second-,
pseudo-first- or pseudo-second order kinetic equation (Chojnacka,
2010; Chojnacka et al., 2005).
The reaction order is related with the mechanism of biosorption,
which is the most frequently ion exchange or surface precipitation
(metal hydroxide, sulfide or carbonate). Literature reports that the
rate limiting step is chemisorption which involves valent forces by
sharing or exchange of electrons between sorbent and sorbate. In
kinetics modeling, Lagergren pseudo-first order and pseudo-second
order models are used (Chojnacka, 2010; Chojnacka et al., 2005):
ln
qeq −qt
= −k1 t; k1 ð1 = minÞ - assumes that metal cation binds only to
qeq
one sorption site on the sorbent surface:
R(s) + Me2+(aq) = RMe2+(ads)
t
qt = 1
k2 q2eq
+ t
qeq ; k2 ðg = mg minÞ - metal cations are bound to two binding
sites on the sorbent surface 2R(s) + Me2+(aq) =
R2Me2+(ads)
If searching for new biosorbents, usually biosorption isotherms are
plotted. The course of the isotherms varies. The mostly advantageous
are those which are steep in the initial course, because if the method is
intended to be used as the final step, the residual concentration of
sorbate would be very low, on the level of a fraction of mg/l. At such
low concentration it is advantageous to reach possibly high sorption
capacity. Of course, the maximum sorption capacity is also an
important model parameter which determines the selection of a
given biosorbent.
Nowadays, many research papers on biosorption discuss multi-
metal biosorption (Aksu and Dönmez, 2006). Many models have been
proposed (Table 3), but so far no universal model has been elaborated.
This is a severe limitation for the practical application of the process,
because multi-metal models describe selectivity of the biosorbent to
sorbate and make it possible to predict the course of the process. In
this field more research needs to be done.
Biosorption can be carried out either by immobilized biomass or in
suspension. Literature reports that immobilization improves mechan-
ical strength, rigidity, porosity and the overall metal ions removal
capacity, as well as life time of the biosorbent. Polymeric matrices used
in biosorbent immobilization include polysulfone, polyurethane, algi-
nate, polyacrylamide, polyethyleneimine (Rangsayatorn et al., 2004).
Literature describes many examples of immobilization: Chlorella
homosphaera - sodium alginate, Sargassum fluitans and Ascophyllum
nodosum - cross-linked with formaldehyde, glutaraldehyde, or poly-
ethylene imine, Sphagnum peat moss - in porous polysulfonate beads,
303
Rhizopus arrhizus - in reticulated polyurethane foam, fungus P.
chrysogenum (a waste from the production of antibiotics) - modified
polyacrylonitrile (Loukidou and Zouboulis, 2005).
In industrial practice it is recommended that a system of parallel
columns packed with immobilized biosorbent operates. While the
first column works and treats wastewater, the other one is
regenerated (Volesky and Schiewer, 2000). In suspended biomass
biosorption system, a biosorber which is stirred tank reactor is used.
The process is very simple, when considering operational aspects,
however in this case it is necessary to add additional biomass-liquid
separation unit which can be clarifier, filter or membrane (micro-
filtration or ultrafiltration).
Also, the possibility of desorption of bound ions from the biomass
and subsequent reuse in another sorption cycle was investigated. The
efficient sorbent that was identified was 0.1 M nitric acid. The
application of 0.1 M acid solution assured almost complete desorption
of bound cations from the biomass with the simultaneous restoration
of sorption properties. Also, the effect of pH on biosorption
performance was studied. This furtherly confirmed the participation
of cation-exchange with functional groups in the biosorption process
(Chojnacka, 2010; Chojnacka et al., 2005). Working on at least two
biosorption columns enables to switch between sorption and
desorption (sorbent regeneration) process without the necessity of
stopping the process. The possibility of sorbent regeneration is an
economic solution. Very significant is to select the proper filtration
device that enables to work at high fluxes over long period of time
(Volesky and Schiewer, 2000).
Biosorption can be performed by immobilized biosorbents.
Disadvantages include additional costs, higher mechanical diffusion
resistance, lower capacity, interaction of carrier with active sites. An
alternative solution would be a membrane reactor which assures
confined space for free cells and enables continuous separation of the
biomass from the solution (Veglio and Beolchini, 1997; Chojnacka,
2010).
3. Technology and commercial applications
The process of biosorption has been recently commercialized and
accepted by EPA (EPA/540/S5-90/005). There are some commercial
biosorbents available on the market: AlgaSORB® and AMT-BIO-
CLAIM®. AlgaSORB® is produced by the company Biorecovery
Systems. This is powdered algal sorbent, 1-3 mm, which is sold for
the price of 28 €. The sorbent consists of the biofilm of immobilized in
silica gel, consisting of filamentous multi-cellular green alga Spirogyra
(Singh and Prasad, 2000). The company Resource Management &
Recovery offers commercial portable systems for biological sorption,
consisting of two columns, each containing 7 L of the biosorbent. The
company declares wastewater treatment efficiency of 0.5 L/min and
that it is possible to construct larger systems with 100 times higher
treatment efficiency by implementing larger columns or adding
additional columns to the system (http://www.clu-in.org/products/
site/complete/resource.htm).
The other commercial preparations for biosorption include: BIO-
CLAIM® (bacteria of the genus Bacillus treated with caustic soda (to
enhance metal-binding), washed, immobilized in extruded beads –
polyethyleneimine (PEI) and glutaraldehyde), BIO-FIX® process
(sphagnum, peat moss, algae, yeast, bacteria and aquatic flora
immobilized in polysulfone) MetaGeneR and RAHCO Bio-Beads (treat-
ment if electroplating and mining waste streams; undergone laboratory
and field trials).
In order to make a technology from the biosorption, some
additional works are required, in particular it is necessary to construct
more pilot plants. This is being done, with various biological sorbents
(Wagner-Dobler, 2003). Also some experiments on scale transfer are
needed (Tsezos, 2001). It is necessary to make more comparisons
with the competing technologies: conventional ion-exchange, reverse
304 K. Chojnacka / Environment International 36 (2010) 299–307

Table 3
Different Langmuir and Freundlich-type equations used in modeling multi-metal biosorption.

Model Name Decription Ref.

Equations based on Langmuir model

q bC
qi;eq = max;iN i i;eq the predictive competitive derived from corresponding individual Lanmguir isotherms; assumes the same selectivity, 1, 4-5)
1 + ∑ bj Cj;eq
j=1 Langmuir model uniform surface and that all cations compete for the same binding sites without interaction
nor competition between ions; qmax is determined from single metal system and theoretically
should be the same for all metal cations; if qmax differs, this means that binding sites are not
homogeneous and are specific towards metal cations; but this is not consistent with the basic
Ci;eq assumption of Langmuir equation; if sorbent shows heterogeneity, then affinity should differ
qmax;i bi ηi
qi;eq = N Cj;eq
empirical extension beside mono-component coefficients, additional competition coefficients are determined from 3-5)
1 + ∑ bj
j=1
ηj Langmuir model experimental multi-metal data; non-ideal competition between sorbates is assumed; the model
is more flexible and represents complexity of multi-metal system; qmax is general for various
multi-component systems
Qmax;i Bi Ci;eq
qi;eq = N Langmuir model all parameters are determined by fitting to multi-component equilibrium data 5)
1 + ∑ Bj Cj;eq
j=1

qmax;Total bi Ci;eq
qi;eq = N Langmuir model with general general total binding capacity (qmax,Total) and additional correction coefficients (η) are used in 4)
1 + ∑ η jbj Cj;eq
j=1 total binding capacity this isotherm; the total binding capacity is the same for all the cations and can be determined by
potentiometric titration (total active site concentration or total cation exchange capacity); total
metal uptake at given pH is constant for all the cations; if pH decreases, binding capacity also
i n decreases; all the cations compete for the same binding sites
qmax;i bi Ci;eq
qi;eq = N n
extension Langmuir- artificial neural networks were used to solve this equation 6)
j
1 + ∑ bj Cj;eq
j=1 Freundlich model
ðqmax;i −qmax; j Þbi Ci;eq qmax; j bi Ci;eq
qi;eq = 1 + bi Ci;eq
+ N (qmax,i – qmax, j)- the fraction of ions which adsorb without competition 2)
1 + ∑ bjCj;eq
j=1 qmax, j- the fraction of ions which adsorbs with competition

Equations based on Freundlich model

in + n1
KF Ci;eq
qi;eq = N n
the predictive competitive KF,i and ni are determined from individual Freundlich isotherms; 3)
n1 + ∑ b C j
Ci;eq j j;eq
j=1 Freundlich model
n0 + ni1
i
KF;i Ci;eq
qi;eq = N n
empirical extension KF,ij, nij are correction coefficients determined in multi-metal system 3)
ni1 ij
Ci;eq + ∑ KF;ij Cj;eq
j=1 Freundlich model

1) Bellot and Condoret, 1993.

2) Jain and Snoeyink, 1973.
3) Pagnanelli et al., 2001.
4) Pagnanelli et al., 2002.
5) Pagnanelli et al., 2004.
6) Chu and Kim, 2006.

osmosis, with a particular impact on the costs of biosorbents
formulation into ready-to-use products (Volesky, 2007). It is also
necessary to make some market studies, to identify the potential
customers and to convince them about the advantages offered by the
use of renewable sorbents (Volesky, 2007).
4. Bioaccumulation
Bioaccumulation is defined as intracellular accumulation of sorbate,
which occurs in two-stages: the first identical with biosorption which is
quick, and the subsequent, which slower and includes transport of
sorbate into inside of cells by - the most frequently - active transport
system (Table 4, Fig. 2). Bioaccumulation is non-equilibrium process
(Aksu and Dönmez, 2000).
The process is more complex than biosorption itself and requires
metabolic activity of cells. It can be defined as the cultivation of an
organism in the presence of sorbate. There are examples where the
process of bioaccumulation is supported by metabolic processes. This
happens in the case of algae which intake gaseous CO2 as the source of
carbon for growth but the substrate present in the growth medium is
bicarbonate. The following reaction proceeds in the vicinity of the cell
wall (Fig. 3):
 
HCO3 →CO2 þ OH
For this reason in the vicinity of cell surface, increased concentrations
of hydroxide ions are found. This favors precipitation of hydroxides of
toxic metals and support wastewater treatment processes.
In other cases, different metabolic processes participate in the
removal of toxic metal ions (Table 4): extracellular metabolic
transformations (biotransformations, biomineralization – the formation
of insoluble sulfides or phosphates by the release of, respectively, sulfide
or phosphate ions by the cell (Gavrilescu, 2004; Lloyd, 2002). This
property is used in the removal of ions of Fe, Mn and Pb (Loukidou and
Zouboulis, 2005).
When considering the operational aspects, bioremoval by growing
cells is usually performed in batch systems (Aksu and Dönmez, 2000).
The advantage of the process of bioaccumulation, is that it is not
necessary to include a separate biomass cultivation mode nor harvesting
biomass from the environment. Also, additional unit processes are
reduced: harvesting, drying, processing and storage (Aksu and Dönmez,
2005). The process of bioremoval of pollutants is highly affected by the
operational conditions, in particular by the presence of pollutants in the
growth medium which can inhibit the growth of cells and also
bioaccumulation itself. This is a severe limitation of the process, because
it makes it impossible to treat solution with high load of pollutants.
Moreover, it is necessary to supply external source of energy to growing
cells (eg. sucrose from molasses) (Aksu and Dönmez, 2005). However, if
the proper strains are selected, it is possible to propose a self-
replenishing system (Aksu and Dönmez, 2005), whereby biological
material which accumulate pollutants (either inorganic ions or organic
compounds) becomes generated in bioaccumulation unit. Hope for the
practical application of bioaccumulation is that the majority of
conventional municipal wastewater treatment plants bases on living
organisms, with a significant contribution of bioaccumulation itself
(Aksu and Dönmez, 2000). Although, this contribution has not been
investigated thoroughly, yet.
 K. Chojnacka / Environment International 36 (2010) 299–307 305

Table 4
Some facts on bioaccumulation and the mechanisms supporting bioremoval.

Bioaccumulation (Wang and Chen, 2006; Vieira and
Volesky, 2000; Davis et al., 2003; Aksu, 2005):
Other mechanisms supporting bio-removal of metals
(Naja and Volesky, 2010):
– Intracellular accumulation of metals
– Metabolism- and energy- dependent process
– Requires active respiration
– Usually slower than adsorption
– In some cases: more metal is bound
– In Pseudomonas aeruginosa
– I – passive
– II – active - exchange of Cu(II) ions with Ca(II) and Mg(II) across the cell wall.; metal ions are transferred to
the interior of cells by energy systems associated with eg. Mg(II)/K(I) transport (eg. in Pseudomonas, Thiobacillus)
– Metabolic processes may affect physico-chemical biosorption and bioavailability of the substance
– Excreted products
– Higher complexity
– Influence of metabolic processes on sorption – unappreciated
– Degradation of organic pollutants and sorption, transport, complex and transport metals, metalloids and
radionuclides... contribute to the overall treatment.
– Advantageous if simultaneous biodegradation of organic matter required.
– precipitation of MnO2 by aerobic heterotrophs
– microbial decomposition of organic matter with the formation of NH3 and HCO-3, which causes pH increase and
consequently the formation of oxyhydroxides of Fe, Mn and Al in aerobic zones with co-precipitation
– the formation of H2S under anoxic conditions
– production of alkalinity
– oxidation of organic matter by sulfate (e- acceptor → H2S): sulfate reduction, iron monosulfate formation,
the formation of insoluble pyrite

In bioaccumulation pollutants are transported across cell wall and
membrane. Inside the cells are bound to intracellular structures
(Kujan et al., 1995). Literature lists the following processes contrib-
uting to the mechanism of bioaccumulation: including intracellular
accumulation and oxidation or reduction reactions (Yilmazer and
Saracoglu, 2009). The process is very complex and depends of several
factors (which are almost identical as the factors influencing the
cultivation of an organism): the composition of the growth medium
or in other words, in this case – wastewater, pH, temperature, the
presence of other pollutants (which are growth inhibitors, as well) or
other inhibitors, surfactants etc. (Kujan et al., 1995).
Toxic metal ions form complexes with cellular membrane. This
causes the loss of its integrity and impairs its function (Yilmazer and
Saracoglu, 2009). It was found that increasing the concentration of
pollutant which is to be accumulated poses changes in morphology and
physiology of cells (de Siloniz et al., 2002). If toxic metal ions are present
with the cell, they pose toxicity which results from interactions of toxic
metal ions with sulphydryl groups of enzymes. On the other hand, the
process of bioaccumulation is supported by synthesis of low molecular
weight proteins metallothioneins, which are rich in thiol groups (from
eg. cysteine), binding them in the form which is not active biologically
and thus is excluded from metabolical reactions. These proteins bind
Fig. 3. Mechanisms supporting bioaccumulation in algae.
metal ions and are frequently synthesized as the response to the
presence of metal ions in the growth medium, being induced by the
presence of these pollutants (Martin-Gonzalez et al., 2006). This
explains why many reports show that bioaccumulation by adapted
microorganisms is more efficient than by non-adapted (Kocberber and
Donmez, 2007; de Siloniz et al., 2002). Efficient bioaccumulation is also
achieved by species isolated from polluted environments (Kocberber
and Donmez, 2007). There are studies which employ genetically
engineered microorganisms. Deng and Wilson (2001) used Escherichia
coli plasmid from pea with genes of metallothionein, which improved
bioaccumulation of mercury.
Literature widely discusses bioaccumulation of toxic metal ions and
dyes by growing yeast. Yeast are chosen because can be obtained at
almost no cost as industrial by-product from fermentation industry. It
was found that yeast are efficient in accumulation of both metal ions and
organic compounds (Aksu and Dönmez, 2005). Removal of color from
effluents is of particular importance, since photosynthetic activity is
inhibited in the colored waters (Dönmez, 2002). Problematic is that
dyes are frequently non-biodegradable compounds, so it is advanta-
geous to use either biosorption or bioaccumulation processes (Aksu and
Dönmez, 2005). Many strains of fungi were discussed in the literature as
being useful for decolorization processes. Aksu (2003) carried out
studies on bioaccumulation of reactive textile dyes by Saccharomyces
cerevisiae in batch system. The effect of the type of dye and its
concentration, together with pH on bioaccumulation were tested. The
best bioremoval performance was achieved at low concentrations of the
dyes (Aksu, 2003). Dönmez described the process of bioaccumulation of
various textile dyes (Remazol Blue, Reactive Black and Reactive Red) by
Candida tropicalis. Bioaccumulation capacity was as follows: 112 mg/g,
202 mg/g and 79 mg/g, respectively. It was found that at higher
concentration of dyes growth of yeast was inhibited. The substrate for
the cultivation was molasses (Dönmez, 2002). The same substrate was
used in the process of copper(II) bioaccumulation by Kluyveromyces
marxianus (Aksu and Dönmez, 2000). There are also many works on
bioaccumulation of metal ions by growing yeast. Dönmez and Aksu
(1999) reported bioaccumulation of Cu(II) by various strains of yeast
Saccharomyces cerevisiae, Kluyveromyces marxianus, Schizosaccharo-
myces pombe and Candida sp. It was found that bioaccumulation was
dependent on the initial concentration of Cu(II) and also on pH. The best
bioaccumulators were found to be Candida sp. and K. marxianus.
Yilmazer and Saracoglu (2009) studied both biosorptive and bioaccu-
mulative properties of Cu(II) and Cr(III) (the uptake capacity was 16 and
306 K. Chojnacka / Environment International 36 (2010) 299–307
9 mg/g, respectively) ions by yeast Pichia stiptis, by non-adapted and
adapted cells. Kujan et al. (1995) reported bioaccumulation of Cd(II)
ions by growing yeast Candida utilis and the process was found to be
dependent on the growth substrate – the source of organic carbon.
Bioaccumulation capacity, if glucose was used as the source of organic
carbon was ten times higher than if xylose was present in the growth
medium (Kujan et al., 1995). Also bioaccumulation properties of other
yeast strains were investigated. de Siloniz et al. (2002) studied
bioaccumulation of Cu(II) by yeast Pichia guilliermondii, which is an
organism isolated from sewage sludge. Bioaccumulation capacity
reached 20 mg/g. The authors compared the process of Cu(II) ions
removal by both living and non-living (biosorption) cells. Ksheminska
et al. (2005) checked bioaccumulation properties of Cr(III) and (VI) of 51
strains of yeast. Bioaccumulation capacities and tolerances towards
metal ions were found to be similar. Al-Saraj et al. (1999) immobilized
growing yeast in sol-gel matrix and used the formulated biogel for the
removal of Hg(II), Zn(II), Pb(II), Cd(II), Ni(II), Cu(II) ions from solutions.
It was confirmed that siloxane sol-gel matrix contained living cells
which were uniformly distributed and accumulated toxic metal ions.
The process was compared with free cells. Several advantages of sol-gel
system were underlined (Al-Saraj et al., 1999).
Other bioaccumulating organisms are aquatic plants – free-floating,
emergent or submerged macrophytes (Kara, 2004). Kara (2004)
investigated the process of bioaccumulation of Cu(II) ions from
wastewater by Lemna minor. This aquatic plant is also capable of the
removal of Cd and Se ions from solutions. Peng et al. (2008) studied
bioaccumulation of Cd(II), Pb(II), Cu(II), Zn(II) and Mn(II) ions by
aquatic plants Potamogeton pectinatus L. and Potamogeton malaianus
Mig. The plants accumulated up to 16 mg/g metals and removal
efficiency reached 67-92%.
5. Conclusions
Both processes, biosorption and bioaccumulation, are in fact a part
of all currently used bioremediation technologies. The processes itself
have the potential to find a practical application in the future
separation technologies, becoming a part of hybrid or integrated
installations for wastewater treatment. However, some more research
is required in this field: it is necessary to furtherly search for better
and more selective biosorbents, to elaborate new, universal biosorp-
tion models for multi-metal systems, to make some more market and
economic studies to be able to evaluate the real investment and
operation costs of biosorption and bioaccumulation wastewater
treatment processes. It is also possible to elaborate artificial materials
which would imitate biosorbents but would not show those
disadvantages which biosorbents have – short life time.
Perhaps the future application of biosorption and bioaccumulation
would lie not in wastewater treatment processes but in the
production of high value products. It is possible to treat the biomass
as the source of specific binding molecules which could be used in
separation of precious biomolecules from the mixture. This would
enable to reduce the number of conventionally used separation steps
and would enable a single-step recovery. Some attempts have been
done in the past in the separation of gold from sea water. But the same
property can be used towards biomolecules (Volesky, 2003).
Another possibility is the use of biomass as the carrier of highly
available microelements in livestock diet, substituting microelements
supplemented in the form if inorganic salts with the form bound with
the biomass by either the process of biosorption or bioaccumulation. In
this case a stress would be on biobinding, not bioremoval (Chojnacka,
2010).
Acknowledgments
The work was financially supported by Polish Ministry of Science
and Higher Education, project nr N 204 019135.
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