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Bioresource Technology 98 (2007) 2243–2257

Review

Microbial and plant derived biomass for removal of


heavy metals from wastewater
Sarabjeet Singh Ahluwalia, Dinesh Goyal *

Department of Biotechnology & Environmental Sciences, Thapar Institute of Engineering & Technology, Patiala 147 004, Punjab, India

Received 12 July 2005; received in revised form 29 November 2005; accepted 2 December 2005
Available online 19 January 2006

Abstract

Discharge of heavy metals from metal processing industries is known to have adverse effects on the environment. Conventional treat-
ment technologies for removal of heavy metals from aqueous solution are not economical and generate huge quantity of toxic chemical
sludge. Biosorption of heavy metals by metabolically inactive non-living biomass of microbial or plant origin is an innovative and alter-
native technology for removal of these pollutants from aqueous solution. Due to unique chemical composition biomass sequesters metal
ions by forming metal complexes from solution and obviates the necessity to maintain special growth-supporting conditions. Biomass of
Aspergillus niger, Penicillium chrysogenum, Rhizopus nigricans, Ascophyllum nodosum, Sargassum natans, Chlorella fusca, Oscillatoria
anguistissima, Bacillus firmus and Streptomyces sp. have highest metal adsorption capacities ranging from 5 to 641 mg g 1 mainly for
Pb, Zn, Cd, Cr, Cu and Ni. Biomass generated as a by-product of fermentative processes offers great potential for adopting an econom-
ical metal-recovery system. The purpose of this paper is to review the available information on various attributes of utilization of micro-
bial and plant derived biomass and explores the possibility of exploiting them for heavy metal remediation.
 2005 Elsevier Ltd. All rights reserved.

Keywords: Biosorption; Non-living microbial biomass; Wastewater; Heavy metals

1. Introduction ery. These processes may be ineffective or extremely expen-


sive especially when the metals in solution are in the range
Increased use of metals and chemicals in process indus- of 1–100 mg l 1 (Nourbakhsh et al., 1994). Another major
tries has resulted in generation of large quantities of efflu- disadvantage with conventional treatment technologies is
ent that contain high level of toxic heavy metals and the production of toxic chemical sludge and its disposal/
their presence poses environmental–disposal problems treatment becomes a costly affair and is not eco-friendly.
due to their non-degradable and persistence nature. In Therefore, removal of toxic heavy metals to an environ-
addition mining, mineral processing and extractive-metal- mentally safe level in a cost effective and environment
lurgical operations also generate toxic liquid wastes. Envi- friendly manner assumes great importance.
ronmental engineers and scientists are faced with the In light of the above, biological materials have emerged
challenging task to develop appropriate low cost tech- as an economic and eco-friendly option. Biomaterials of
nologies for effluent treatment. Conventional methods for microbial and plant origin interact effectively with heavy
removing metals from aqueous solutions include chem- metals. Metabolically inactive dead biomass due to their
ical precipitation, chemical oxidation or reduction, ion unique chemical composition sequesters metal ions and
exchange, filtration, electrochemical treatment, reverse metal complexes from solution, which obviates the neces-
osmosis, membrane technologies and evaporation recov- sity to maintain special growth-supporting conditions.
Metal-sorption by various types of biomaterials can find
*
Corresponding author. enormous applications for removing metals from solution
E-mail address: d_goyal_2000@yahoo.com (D. Goyal). and their recovery.

0960-8524/$ - see front matter  2005 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biortech.2005.12.006
2244 S.S. Ahluwalia, D. Goyal / Bioresource Technology 98 (2007) 2243–2257

Rather than searching thousands of microbial species wastewater. Current research activity in this field is focused
for particular metal sequestering features, it is beneficial on evaluating, whether biosorption may eventually provide
to look for biomasses that are readily available in large such an effective and economic alternative treatment pro-
quantities to support potential demand. While choosing cess, while biological treatment is reasonably effective in
biomaterial for metal sorption, its origin is a major factor removing organic pollutants, heavy metals however tend
to be taken into account, which can come from (a) micro- to accumulate in biological sludge, which is unfit as fertil-
organisms as a by-product of fermentation industry, (b) izers and require incineration for its disposal (Tien and
organisms naturally available in large quantities in nature Huang, 1991).
and (c) organisms cultivated or propagated for biosorption
purposes using inexpensive media. Different non-living bio- 3. Conventional methods for heavy metal removal
mass types have been used to adsorb heavy metal ions from from industrial effluents
the environment (de Rome and Gadd, 1991; Tiemann
et al., 1999). Seaweed, mold, bacteria, crab shells and yeast To mitigate the heavy metal pollution, many processes
are among the different kinds of biomass, which have been like adsorption, precipitation, coagulation, ion exchange,
tested for metal biosorption or removal (Volesky and cementation, electro-dialysis, electro-winning, electro-coagu-
Holan, 1995). lation and reverse osmosis have been developed.

2. Metals in wastewater and their toxicity 1. Precipitation is the most common method for removing
toxic heavy metals up to parts per million (ppm) levels
Effluents from textile, leather, tannery, electroplating, from water. Since some metal salts are insoluble in water
galvanizing, pigment and dyes, metallurgical and paint and which get precipitated when correct anion is added.
industries and other metal processing and refining opera- Although the process is cost effective its efficiency is
tions at small and large-scale sector contains considerable affected by low pH and the presence of other salts (ions).
amounts of toxic metal ions. These toxic metals ions are The process requires addition of other chemicals, which
not only potential human health hazards but also to finally leads to the generation of a high water content
another life forms. Toxic metal ions cause physical dis- sludge, the disposal of which is cost intensive (Gray,
comfort and sometimes life-threatening illness including 1999). Precipitation with lime, bisulphide or ion
irreversible damage to vital body system (Malik, 2004). exchange lacks the specificity and is ineffective in
From the eco-toxicological point of view, the most danger- removal of the metal ions at low concentration.
ous metals are mercury, lead, cadmium and chromium(VI). 2. Ion exchange is another method used successfully in the
In many instances the effect of heavy metals on human is industry for the removal of heavy metals from effluents.
not well understood. Metal ions in the environment bio- Though it is relatively expensive as compared to the
accumulate and are biomagnified along the food chain. other methods, it has the ability to achieve ppb levels
Therefore, their toxic effect is more pronounced in animals of clean up while handling a relatively large volume.
at higher trophic levels. Mine tailing and effluents from An ion exchanger is a solid capable of exchanging either
non-ferrous metals industry are the major sources of heavy cations or anions from the surrounding materials. Com-
metals in the environment (Moore and Ramamoorthy, monly used matrices for ion exchange are synthetic
1984). Among commonly used heavy metals, Cr(III), Cu, organic ion exchange resins. The disadvantage of this
Zn, Ni and V are comparatively less toxic then Fe and method is that it cannot handle concentrated metal solu-
Al. Cu is mainly employed in electric goods industry and tion as the matrix gets easily fouled by organics and other
brass production. Major applications for Zn are galvaniza- solids in the wastewater. Moreover ion exchange is non-
tion and production of alloys (Volesky and Schiewer, selective and is highly sensitive to pH of the solution.
2000). Cadmium has a half-life of 10–30 years (Moore 3. Electro-winning is widely used in the mining and metal-
and Ramamoorthy, 1984) and its accumulation in human lurgical industrial operations for heap leaching and acid
body affects kidney, bone and also causes cancer and its mine drainage. It is also used in the metal transforma-
use is increasing in industrial applications such as electro- tion and electronics and electrical industries for removal
plating and making pigments and batteries. Chromium and recovery of metals. Metals like Ag, Au, Cd, Co, Cr,
compounds are nephrotoxic and carcinogenic in nature Ni, Pb, Sn and Zn present in the effluents can be recov-
(Chen and Hao, 1998). As a result of increasing awareness ered by electro-deposition using insoluble anodes (Gray,
about the toxicity of Hg and Pb, their large-scale use by 1999).
various industries has been either curtailed or eliminated 4. Electro-coagulation is an electrochemical approach,
(Volesky and Schiewer, 2000). An effluent treatment facil- which uses an electrical current to remove metals from
ity within the industry discharging heavy metals contami- solution. Electro-coagulation system is also effective in
nated effluent will be more efficient than treating large removing suspended solids, dissolved metals, tannins
volumes of mixed wastewater in a general sewage treatment and dyes. The contaminants presents in wastewater are
plant. Thus it is beneficial to devise separate treatment pro- maintained in solution by electrical charges. When these
cedures for scavenging heavy metals from the industrial ions and other charged particles are neutralized with
S.S. Ahluwalia, D. Goyal / Bioresource Technology 98 (2007) 2243–2257 2245

ions of opposite electrical charges provided by electro- • Metal can be desorbed readily and then recovered if the
coagulation system, they become destabilized and pre- value and amount of metal recovered are significant and
cipitate in a stable form. if the biomass is plentiful, metal-loaded biomass can be
5. Cementation is a type of another precipitation method incinerated, thereby eliminating further treatment.
implying an electrochemical mechanism in which a
metal having a higher oxidation potential passes into
solution e.g. oxidation of metallic iron, Fe(0) to ferrous 4.2. Disadvantages
iron(II) to replace a metal having a lower oxidation
potential. Copper is most frequently separated by • Early saturation can be problem i.e. when metal interac-
cementation along with noble metals such as Ag, Au tive sites are occupied, metal desorption is necessary
and Pb as well as As, Cd, Ga, Pb, Sb and Sn can be prior to further use, irrespective of the metal value.
recovered in this manner. • The potential for biological process improvement (e.g.
6. Reverse osmosis and electro-dialysis involves the use of through genetic engineering of cells) is limited because
semi-permeable membranes for the recovery of metal cells are not metabolizing. Because production of the
ions from dilute wastewater. In electro-dialysis, selective adsorptive agent occurs during pre-growth, there is no
membranes (alternation of cation and anion mem- biological control over characteristic of biosorbent. This
branes) are fitted between the electrodes in electrolytic will be particularly true if waste biomass from a fermen-
cells, and under continuous electrical current the associ- tation unit is being utilized.
ated ion migrates, allowing the recovery of metals. • There is no potential for biologically altering the metal
valency state. For example less soluble forms or even
for degradation of organometallic complexes.
4. Biosorption
Biosorption is a rapid phenomenon of passive metal uptake
Biosorption is a property of certain types of inactive, sequestration by non-growing biomass (Beveridge and
non-living microbial biomass to bind and concentrate Doyle, 1989). Results are convincing and binding capacity
heavy metals from even very dilute aqueous solution. of certain biomass is comparable with the commercial
Biomass exhibits this property, acting just as chemical synthetic cation exchange resins (Wase and Foster, 1997).
substance, as an ion exchanger of biological origin. It is Volesky and Holan (1995) have reviewed the exhaustive list
particularly the cell wall structure of certain algae, fungi of microbes and their metal binding capacities. Further,
and bacteria, which was found responsible for this phe- sorption capacity is evaluated by sorption isotherms
nomenon (Volesky, 1990). Till now, research in the area described by Langmuir and Freundlich models. The uptake
of biosorption suggests it an ideal alternative for decon- of metal by two biosorbents must be compared at the
tamination of metal containing effluents. Advantages and same equilibrium concentration. The adsorption is easy
disadvantages of biosorption by non-living biomass are to understand when it refers to a single metal situation;
as follows (Modak and Natarajan, 1995). however in a multi-ion situation, which is generally
encountered in effluent, the assessment of sorption becomes
4.1. Advantages complicated. Most of the work exists with single metal
solution and realistic approach would be inferring results
• Growth-independent, non-living biomass is not subject in mixed metal solution at extreme pH and variable metal
to toxicity limitation of cells. No requirement of costly concentration. Biosorption efficiency depends upon many
nutrients required for the growth of cells in feed solu- factors, including the capacity, affinity and specificity of
tions. Therefore, the problems of disposal of surplus the biosorbents and their physical and chemical conditions
nutrients or metabolic products are not present. in effluents.
• Biomass can be procured from the existing fermentation
industries, which is essentially a waste after ferment- 5. Mechanism of metal uptake
ation.
• The process is not governed by the physiological con- The understanding of the mechanism by which microor-
straint of living microbial cells. ganisms accumulate metals is crucial to the development of
• Because of non-living biomass behave as an ion exchan- microbial processes for concentration, removal and recov-
ger; the process is very rapid and takes place between ery of metals from aqueous solution. Metabolism-indepen-
few minutes to few hours. Metal loading on biomass is dent metal binding to the cell walls and external surfaces is
often very high, leading to very efficient metal uptake. the only mechanism present in the case of non-living bio-
• Because cells are non-living, processing conditions are mass. Metabolism-independent uptake essentially involves
not restricted to those conducive for the growth of cells. adsorption process such as ionic, chemical and physical
In other words, a wider range of operating conditions adsorption. A variety of ligands located on the fungal walls
such as pH, temperature and metal concentration is pos- are known to be involved in metal chelation. These include
sible. No aseptic conditions are required for this process. carboxyl, amine, hydroxyl, phosphate and sulfhydryl
2246 S.S. Ahluwalia, D. Goyal / Bioresource Technology 98 (2007) 2243–2257

groups. Metal ions could be adsorbed by complexing with when the brown seaweed Sargassum fluitans was exposed
negatively charged reaction sites on the cell surface (Beve- to Fe2+, while only Fe3+ was present when biomass was
ridge and Murray, 1980; Gupta et al., 2000). The relative exposed to ferric ions. Further, FTIR analysis has con-
importance of each functional group is often difficult to firmed that both carboxyl groups were involved in the
resolve (Strandberg et al., 1981). Microbial cell wall is rich uptake of Fe2+ and Fe3+ and sulfonate groups were
in polysaccharide and glycoproteins such as glucans, chitin, responsible for Fe3+ uptakes.
mannans and phospho-mannans. These polymers form
abundant source of metal binding ligands. Cell walls of 6. Removal of metal by non-living biomass of microbial and
fungi present a multi-laminate architecture where up to plant origin
90% of their dry mass consists of amino or non-amino
polysaccharides (Farkas, 1980). In general, the fungal cell Removal of heavy metals from aqueous solution by
wall can be regarded as a two-phase system consisting of using inactive and dead biomass is an innovative and alter-
the chitin skeleton framework embedded in an amorphous native technology for removing these pollutants. Non-
polysaccharide matrix (Farkas, 1980). Up to 30% of Asper- living biomass of algae, aquatic ferns and seaweeds, waste
gillus niger biomass is comprised of an association of chitin biomass originated from plants and mycelial wastes
and glucan (Muzzarelli and Tanfari, 1982). Chitin and (Tables 1a–1c and 1d) from fermentation industries are
chitosan components of the cell wall are suggested to be potential biosorbents for removal of heavy metals from
important for metal uptake (Tsezos and Volesky, 1981; aqueous solution and wastewater (Puranik and Paknikar,
Fourest and Roux, 1992). 1999; Ahluwalia and Goyal, 2005). Considerable potential
Muraleedharan and Venkobachar (1990) reported cop- exists for these naturally existing, abundant and cheap
per binding wood-rotting fungi Ganoderma lucidum was sources of biomass, for use as adsorbents. Their efficiency
reduced only marginally when the biosorbent was devoid depends on the capacity, affinity and specificity including
of chitin, indicating that chitin does not play a major role physico-chemical nature. Biomass related metal removal
in the system. Electron paramagnetic-resonance spectra processes may not necessarily replace existing treatment
of biosorbent indicated the presence of a free radical processes but may complement them.
(unidentified) in the cell wall matrix, which interacts with
metal, resulting in metal binding by the cells. Mechanism 6.1. Removal of metals by fungal biomass
of uranium binding Rhizopus arrhizus involves the amine
nitrogen of chitin crystallites and takes place in a sequence Copper biosorption by non-living wood rotting fungus
of events (Tsezos and Volesky, 1982). Other studies in fungi Ganoderma lucidum was studied and it was found that pro-
have implicated the phosphate and carboxylate groups tein interaction with metals did not play a significant role
of the cell wall in primary binding (Akthar et al., 1996; in copper(II) uptake (Muraleedharan and Venkobachar,
Kapoor and Viraraghavan, 1997). 1990). Waste mycelia of A. niger, Phanerochaete chryso-
Determination of the exact mechanism is further com- genum and Claviceps paspali from industrial fermentation
plicated by complex solution chemistry of the metals and plants were used as biosorbent for Zn from aqueous envi-
the inability to determine the precise metal complex present ronments in batch as well as column modes. Under opti-
in the solution (Tobin et al., 1984), which is not readily mized conditions, A. niger and C. paspali were superior
amenable to instrumental analysis (Kuyucak and Volesky, to P. chrysogenum (Luef et al., 1991). Biosorption of lead
1989). Differences in affinities between elements and their by P. chrysogenum biomass was strongly affected by pH.
ionic species may exist for various ligands encountered in At pH 4–5, the saturated uptake capacity for lead sorption
biological system. Cell wall of different fungi can vary con- was higher than that of activated charcoal and that
siderably in their overall composition, which leads to vary- reported for some other organisms (Niu et al., 1993). Dead
ing adsorption capacity. However, localization of metal(s) cells of Saccharomyces cerevisiae removed 40% more ura-
has been carried out using electron microscopic and X- nium or zinc than live cultures and biosorption rapidly
ray energy dispersive analyses. X-ray photoelectron spec- reached 60% of the final uptake value within 15 min of con-
troscopy for chemical analysis is a relatively new technique tact and uranium was deposited as fine needle-like crystals
for determination of binding energy of electrons in atoms/ inside the cells and on the outer cell surface (Volesky and
molecules, which depends upon the distribution of valence May-Phillips, 1995).
charges and thus gives information about the oxidation Non-living waste biomass of A. niger attached to wheat
state of an atom/ion (Gupta et al., 2000). Electron micro- bran was used as a biosorbent for removal of Zn and Cu
scopic observation carried out by Mullen et al. (1989) from aqueous solution and metal uptake was found to be
revealed the presence of Ag2+ as discrete particles at or a function of the initial metal concentration, biomass load-
near the cell wall of both gram-positive and gram-negative ing and pH. Metal uptake decreased in the presence of co-
bacteria. The presence of silver was also confirmed by ions, which was dependent on the concentration of metal
energy dispersive X-ray analysis (EDAX). Figueira et al. ions in two compounds in aqueous solution (Modak
(1999) using the X-ray photoelectron spectroscopy et al., 1996). Alkali treated biomass of A. niger referred
observed that iron was present in two oxidation states, to as Biosorb, was found to sequester Cd2+, Cu2+, Zn2+,
S.S. Ahluwalia, D. Goyal / Bioresource Technology 98 (2007) 2243–2257 2247

Table 1a
Fungal biomass for removal of heavy metals from aqueous solution
Biosorbent Metals Adsorption References
capacity (mg g 1)
Aspergillus foetidus Cr(VI) 2 Prasanjit and Sumathi (2005)
Aspergillus niger Cu 5 Townsley and Ross (1986)
– Modak et al. (1996)
Co 95 Kuyucak and Volesky (1989)
Au 200 Kuyucak and Volesky (1989)
Co 2.4 Sakaguchi and Nakajima (1991)
Cr, Fe – Goyal et al. (2003)
Pb 30 Kim et al. (1995)
Th 22 Tsezos and Volesky (1981)
162 Gadd (1988)
U 29 Sakaguchi and Nakajima (1991)
27 Kuyucak and Volesky (1989)
Zn – Luef et al. (1991),Modak et al. (1996),
Muter et al. (2002)
Aspergillus terreus Th, U 60, 10 Tsezos and Volesky (1981)
Aureobasidium pullulans Cu 6 Gadd and Mowll (1995)
Pb 56.9 Suh et al. (1998)
– Ahluwalia and Goyal (2003)
Cladosporium resinae Cu 18 Gadd (1988)
de Rome and Gadd (1987)
Pb – Ahluwalia and Goyal (2003)
Candida utilis Cr, Cu, Pb – Muter et al. (2002)
Ganoderma lucidum Cu 24 Muraleedharan and Venkobachar (1990)
Mucor meihi Cr – Tobin and Roux (1998)
Mucor rouxii Pb, Zn, Cd, Ni 17, 4.89, 6.94, 5.24 Yan and Viraraghavan (2003)
Pb 769 Lo et al. (1999)
Penicillium chrysogenum Cd, Cu, Pb 11, 9, 116 Niu et al. (1993)
Cd 56 Holan and Volesky (1995)
39 Fourest et al. (1994)
Th 142 Tsezos and Volesky (1981)
Gadd and White (1992)
U 70 Tsezos and Volesky (1981)
Zn 6.5 Niu et al. (1993)
– Luef et al. (1991)
Cd, Zn, Cu, Pb – Skowroñski et al. (2001)
Pleurotus sapidus Cd, Hg 127, 287 Yalcinkaya et al. (2002)
Streptoverticillium cinnamoneum Pb, Zn 57.7, 21.3 Puranik and Paknikar (1997)
Penicillium italicum Cu – de Rome and Gadd (1987)
Th – Gadd and White (1989)
Penicillium spinulosum Cu, Zn 0.4–2, 0.2 Townsley and Ross (1985)
Phanerochaete chrysosporium Cd 84.5 Gabriel et al. (1996)
Pb 2 Say et al. (2001)
Cu – Yetis et al. (2000)
Rhodotorula glutinis Pb 73.5 Cho and Kim (2003)
Rhizopus nigricans Cr, Pb 47 Bai and Abraham (2001)
Zn 14 Zhang et al. (1998)
Cd, Ni, Pb 19, 5, 166 Fourest and Roux (1992)
Holan and Volesky (1995)
R. oligosporus Cr 126 Ariff et al. (1999)
Cd 17.09 Aloysius et al. (1999)
R. arrhizus Ni, Cd, Zn, Pb, Cu 18, 27, 14, 56, 9.5 Fourest and Roux (1992)
Cd 30 Holan and Volesky (1995)
Cr 11 Bai and Abraham (1998)
36 Nourbakhsh et al. (1994)
Co 2.9 Sakaguchi and Nakajima (1991)
– Niyogi et al. (1998)
– Sag and Kutsal (1998)
– Prakasham et al. (1999)
Cu 10 Gadd (1988)
– de Rome and Gadd (1987),
Sag and Kutsal (1998),
Zhou and Kiff (1991)
(continued on next page)
2248 S.S. Ahluwalia, D. Goyal / Bioresource Technology 98 (2007) 2243–2257

Table 1a (continued)
Biosorbent Metals Adsorption References
capacity (mg g 1)
Th 185 Tsezos and Volesky (1981)
97 Gadd et al. (1988)
– Gadd and White (1992)
U 220 Tsezos and Volesky (1981)
– Tsezos et al. (1989)
– Tsezos and Deutschmann (1990)
Saccharomyces cerevisiae Cd – Volesky et al. (1993)
Cr – Nourbakhsh et al. (1994)
11.4 Omar et al. (1996)
Co 5.8 Sakaguchi and Nakajima (1991)
Pb – Suh et al. (1998)
Th 119 Gadd (1988)
Cu 17–40 Volesky and May-Phillips (1995)
U 55–140
Cu 10 Mattuschka et al. (1993)
0.4 Huang et al. (1990)
Zn 14–40 Volesky and May-Phillips (1995)
Trametes versicolor Cr – Bayramoglu et al. (2003)
Cd 109 Gabriel et al. (1996)

Ni2+ and Co2+ efficiently up to 10% of its weight (w/w) place in the chitin structure of the cell wall (Zhang et al.,
and exhibited higher metal binding capacity as compared 1998).
to Neurospora, Fusarium and Penicillium (Akthar et al., Removal of Cr(VI) from aqueous solution was carried
1996). The kinetics of metal binding by Biosorb indicated out in batch mode using dead biomass of fungal strains
that it is a rapid process and about 70–80% of the A. niger NCIM-501, A. oryzae NCIM-637, R. arrhizus
metal is removed from solution in 5 min followed by slower NCIM-997 and R. nigricans NCIM-880. Basic parameters
rate. such pH (2.0–8.0), initial metal ion concentration (100–
Dry cells of R. arrhizus were used for removal of Fe(II), 500 mg l 1), contact time (2–24 h) and varying biomass
Pb(II) and Cd(II) ions from industrial wastewater (Ozer concentration (0.5–3.0 g) were optimized. R. nigricans
et al., 1997). Higher adsorption rate and adsorption capa- and R. arrhizus possessed good specific uptake of
city were obtained at initial metal concentration up to 11 mg Cr(VI) g 1 of biomass at the pH range of 2.0–7.0.
100 mg l 1 in a batch reactor. Cd(II) biosorption to non- Metal uptake capacity was in the order of Rhizopus nigri-
living biomass of fungus R. arrhizus and green alga Schi- cans > Rhizopus arrhizus > Aspergillus oryzae > Aspergillus
zomeris leiblenii showed that maximum adsorption rate of niger (Bai and Abraham, 1998). Mucor meihi, a fermenta-
Cd(II) ions to microbial biomass was at 30 C and pH tion industry waste was found to be an effective biosorbent
5.0, which increased with increasing Cd(II) concentration for the removal of hexavalent chromium from leather
up to 100–150 mg l 1. Adsorption by R. arrhizus was much industry effluent. In comparative studies with ion-exchange
higher than S. leiblenii (Ozer et al., 1997). Dried, non-liv- resins, Mucor biomass showed biosorption levels corre-
ing, granulated biomass of Streptoverticillium cinnamoneum sponding to the strongly acidic commercial resins.
was used for recovery of Pb and Zn at optimum pH 5.0–6.0 Response to pH was similar to the weakly acidic resins in
and 3.5–4.5, respectively. Maximum loading capacity of S. solution and chromium elution characteristics were similar
cinnamoneum biomass pre-treated with boiling water was to both weakly and strongly acidic resins (Tobin and Roux,
57.7 mg g 1 for Pb and 21.3 mg g 1 for Zn. The metals 1998). Non-living free and immobilized biomass of R.
were effectively desorbed with dilute HCl, nitric acid and arrhizus were used to study biosorption of chromium(VI).
0.1 M EDTA (Ethylene diamine tetra acetic acid). The removal rates were slightly more in free biomass con-
Treatment with 0.1 M sodium carbonate permitted reuse ditions over immobilized state. Stirred tank reactor studies
of desorbed biomass, which decreased loading capacity indicated maximum chromium biosorption at 100 rpm and
by 14–37% in subsequent cycles (Puranik and Paknikar, 1:10 biomass–liquid ratio. The fluidized bed reactor was
1997). Waste mycelial biomass comprising of Rhizopus more efficient in chromium removal than the stirred tank
nigricans from the pharmaceutical fermentation industry, reactor (Prakasham et al., 1999).
was used for adsorption of lead over a range of metal ion The influences of co-cations (cadmium, copper, cobalt
concentrations, adsorption times, pH and co-ions. Uptake and nickel) on lead and zinc biosorption by S. cinnamo-
process followed Langmuir and Freundlich adsorption neum and Penicillium chrysogenum in binary and multi-
isotherms. Comparison of the uptake between NaOH-trea- metal systems was studied (Puranik and Paknikar, 1999).
ted and untreated biomass showed that adsorption took Metal sorption capacity of S. cinnamoneum was observed
S.S. Ahluwalia, D. Goyal / Bioresource Technology 98 (2007) 2243–2257 2249

Table 1b
Algal biomass for removal of heavy metals from aqueous solution
Biosorbent Metals Adsorption capacity (mg g 1) References
Ascophyllum nodosum Cd 215 Holan et al. (1993)
Co 156, 100 Kuyucak and Volesky (1988, 1989)
Ni, Pb 30, 270–360 Holan and Volesky (1995)
Cd 30 Volesky and Prasetyo (1994)
Aphanothece halophytica Zn 133 Incharoensakdi and Kitjaharn (2002)
Chlorella vulgaris Ag – Harris and Ramelow (1990)
Cd 111 Aksu (2001)
Cu 43 Aksu et al. (1992)
Cr 3.5 Nourbakhsh et al. (1994)
Cr, Cu, Ni Donmez et al. (1999)
U 3.95 Sakaguchi and Nakajima (1991)
– Greene et al. (1986)
Chlorella fusca Pb 293 Wehreim and Wettern (1994)
Chlorella sorokiniana Cd – Akhtar et al. (2003)
Cladophora crispate Cr 3 Nourbakhsh et al. (1994)
Caulerpa lentillifera Cu, Cd, Pb, Zn – Apiratikul et al. (2004)
Dunaliella sp. Cr 58.3 Donmez and Aksu (2002)
Fucus vesiculosus Cd 73 Holan et al. (1993)
Ni, Pb 17, 220–371 Holan and Volesky (1995)
Fucus spiralis Cd 64 Cordeo et al. (2004)
Ecklonia maxima Cd – Stirk and Staden (2002)
Laminaria japonica Cd – Yun et al. (2001)
Laurencia obtuse Cr – Hamdy (2000)
Lyngbya taylorii Cd, Pb, Ni, Zn – Klimmek et al. (2001)
Phormidium laminosum Cu, Ni, Zn – Blanco et al. (1998)
Pilayella littoralis Al, Cd, Co, Cr, Ni, Zn – Carrilho and Gilbert (2000)
Pachymeniopis sp. Cr(VI) 225 Lee et al. (2000)
Oscillatoria anguistissima Zn 641 Ahuja et al. (1999)
Zn, Cu, Co – Mohapatra and Gupta (2005)
Spirogyra sp. Cr – Gupta et al. (2001)
Scenedesmus quadricula Cd, Cu, Zn – Harris and Ramelow (1990)
Scenedesmus obliquus Cr, Cu, Ni – Donmez et al. (1999)
Scenedesmus abundans Cd, Cu – Terry and Stone (2002)
Scenedesmus incrassatulus Cr, Cd, Cu – Pena-Castro et al. (2004)
Sargassum fluiyans Cu – Schiwer and Volesky (1996)
51 Kratochvil et al. (1997)
Sargassum natans U – Kuyucak and Volesky (1989)
Cd 135 Holan et al. (1993)
Ni, Pb 24–44, 220–270 Holan and Volesky (1995)
Sargassum sp. Zn – da Cotsa et al. (2001)
Sargassum sp. Cu 38, – Volesky et al. (2003),Padilha et al. (2005)
Cd, Zn, Cu 157, 118, 77 Valdman and Leite (2000)
Cd 120 Cruz et al. (2004)
Tetraselmis suecica Cd – Perez-Rama et al. (2002)
Ulothrix zonata Cu – Nuhoglu et al. (2002)
Ulva lactuca Hg – Zeroual et al. (2003)

to be higher than P. chrysogenum for all metals. The extent ature of 45 C, a contact time of 30 min and a dosage of
of metal sorption depended on metal chemistry, affinity for 0.5% (w/v) with a biomass particle size of 90 lm. High
binding sites and type of metal. The order of metal biosorp- adsorption was observed at lower initial concentration of
tion in a multi-metal system could be predicted well based Cr ions (Bai and Abraham, 2001).
on Langmuir parameters evaluated in binary metal system. The biosorption of Cd(II), Pb(II) and Cu(II) onto the
The kinetics and mechanisms of lead(II) biosorption by dry fungal biomass of Phanerochaete chrysosporium was
pulverized R. oligosporus were studied in batch mode (Ariff investigated from artificial wastewater in the concentration
et al., 1999). At an initial lead concentration ranging from range of 5–500 mg l 1 (Say et al., 2001). Maximum bio-
50 to 200 mg l 1, pH 5.0 and optimum biomass concen- sorption of different heavy metal ions was obtained at
tration (0.5 g l 1) the maximum lead adsorption was pH 6.0 and biosorption equilibrium was established after
750 mg g 1 with lead uptake capacity of 126 mg g 1. Chro- about 6 h and experimental biosorption data followed the
mium sorption by powdered biomass of R. nigricans was Langmuir adsorption model. The biosorption of heavy
optimum at pH 2, an agitation rate of 120 rpm, a temper- metals by whole mycelia and selected components of A.
2250 S.S. Ahluwalia, D. Goyal / Bioresource Technology 98 (2007) 2243–2257

Table 1c
Bacterial biomass used for metal removal
Biosorbent Metals Adsorption capacity (mg g 1) References
Pseudomonas fluorescens Th, U 15, 6 Tsezos and Volesky (1981)
Pseudomonas sp. U – Pons and Fuste (1993)
Ochrobactrum anthropi Cr, Cd, Cu – Ozdemir et al. (2003)
Thiobacillus ferrooxidans Zn 82 Baillet et al. (1998)
Cr – Celaya et al. (2000)
Rhodococcus erythropolis Cd, Zn – Plette et al. (1996)
Ocimum basilicium Cr – Melo and D’Souza (2004)
Sphingomonas paucimobilis Cd – Tangaromsuk et al. (2002)
Bacillus firmus Pb, Cu, Zn 467, 381, 418 Salehizadeh and Shojaosadati (2003)
B. coagulans Cr(VI) 39.9 Srinath et al. (2002)
B. megaterium Cr(VI) 30.7 Srinath et al. (2002)
Zoogloea ramigera Cr(VI) 2 Nourbakhsh et al. (1994)
Cu 29 Aksu et al. (1992)
Streptomyces noursei Cd, Cu, Ni 3.4, 9, 0.8 Mattuschka and Straube (1993)
Pb, Zn, Ag, Co 36, 1.6, 38 Mattuschka and Straube (1993)
Cr, Pb 1.2 Mattuschka and Straube (1993)
1.8, 55 Mattuschka et al. (1993)
S. longwoodensis Pb, U 100, 440 Friis and Myers-Keith (1986)
S. rimosus Zn 30 Mameri et al. (1999)

Table 1d
Plant derived biomass used for metal removal
Biosorbent Metals Adsorption capacity (mg g 1) References
Activated baggase carbon Cr – Mor et al. (2002)
Alfalfa Cu, Pb 20, 43 Tiemann et al. (1999)
Artocarpus heterphyllus Cd – Inbaraj and Sulochana (2004)
Azolla filiculoides Pb 93 Sanyhumbi et al. (1998)
Banana pith (Musacea zingiberales) Pb, Cu, Ni, Cr, Zn – Low et al. (1995)
Hydrilla verticillata casp. and Salvinia sp. Cu – Elankumaran et al. (2003)
Carrot pulp Pb, Ni, Zn, Fe – Joshi et al. (2003)
Ceratophyllum demersum Cu, Pb, Zn 6.17, 45, 14 Keskinkan et al. (2004)
Cupressus Female Cone Cr(VI) 119 Murugan and Subramanian (2003)
Eucalyptus wood powder Pb, Ni, Zn, Fe – Joshi et al. (2003)
Eucalyptus bark Cr(VI) – Sarin and Pant (2006)
Ground corncobs Cd, Cu, Pb – Vaughan et al. (2001)
Ni, Zn –
Hydrilla verticillata casp. Cu – Elankumaran et al. (2003)
Larrea tridenta Cu 24 Gardea-Torresdey et al. (2004a,b)
Olive mill solid residue Hg, Pb, Cu – Pagnanelli et al. (2002)
Zn, Cd – –
Paper mill sludge Pb, Cu, Ag – Calace et al. (2003)
Cd – –
Pb, Ni, Zn, Fe – Joshi et al. (2003),Ahluwalia and Goyal (2004)
Sago processing waste Cu, Pb 12.4, 46.6 Quek et al. (1998)
Sawdust Zn, Ni, Cd, Cu, Pb – Marin and Ayele (2002)
Cr(VI) – Acar and Malkoc (2004)
Wheat stem and Spent Babul Bark Ni – Verma and Shukla (2000)
Oryza sativa L. hush Pb – Zulkali et al. (2006)
Waste tea-leaves Pb, Ni, Zn, Fe – Joshi et al. (2003),Ahluwalia and Goyal (2005)
Wolffia globosa Cd, Cr – Upatham et al. (2002)
Water hyacinth roots Cr – Low et al. (1997)
Helianthus annuus L. (Sunflower) Cu – Lin et al. (2003)
Allium sativum L. (Garlic) Cd – Jiang et al. (2001)
Grape stalk waste Cu, Ni 15.9, 18.1 Villaescusa et al. (2004)
Hemidesmus indicus Pb – Chandrasekhar et al. (2003)
Myriophyllum spicatum Pb, Cu, Cd – Keskinkan et al. (2003)

niger, R. oryzae and Mucor rouxii was studied (Baik et al., considerably improved by treating the cell wall fraction
2002). Binding of copper, cadmium, nickel and zinc was with 4 M NaOH at 121 C.
S.S. Ahluwalia, D. Goyal / Bioresource Technology 98 (2007) 2243–2257 2251

6.2. Removal of metals by algal biomass tion level was found to be a function of contact time at dif-
ferent initial metal ion concentration and the adsorption
Chromium sorption by non-living biomass of Chlorella data showed the Langmuir adsorption model. The free
vulgaris and Cladophora crispata along with bacteria and energy change for the adsorption process was found to
fungi was studied and it was observed that pH affected be 12.60 kJ mol 1. Dried Caulerpa lentillifera was shown
metal uptake capacity (Nourbakhsh et al., 1994). Maxi- to have adsorption potential for Cu, Cd, Pb and Zn (Api-
mum adsorption was observed at a temperature range of ratikul et al., 2004). The adsorption equilibrium followed
25–35 C, which increased with increasing metal concen- the Freundlich isotherm. The adsorption of metals from
trations up to 200 mg l 1. The short-term accumulation binary mixture of heavy metal was competitive and the
of chromate by Anabaena sp. and Synechococcus sp. adsorption capacity of any single metal decreased by 10–
PCC6301 was rapid with relatively low level of sorption 40% in the presence of the other metallic species and the
to the cell wall. The process was not energy dependent overall adsorption capacity of the algae decreased by 30–
but was regulated bychromate concentration described by 50%.
Freundlich adsorption isotherm. On decreasing pH, chro- Uranium biosorption by powered biomass of lake-har-
mate accumulation increased in both the species. Over a vested water bloom cyanobacterium Microcystis aeruginosa
longer growth period Anabaena variabilis was capable of (Li et al., 2004) was optimum at 4.0–8.0 pH. The batch
reducing chromate(VI) to chromium(III) and accumulating sorption reached the equilibrium within 1 h and followed
it. Synechococcus PCC 6301 showed no further interaction the Freundlich isotherm model. Uranium was effectively
with chromate concentration over the same period after an desorbed with 0.01 N HCl. This naturally abundant bio-
initial biosorption (Garnham and Green, 1995). In brown mass otherwise nuisance cyanobacterium exhibited good
seaweeds, 90–95% removal of Hg and Cd from industrial potential for application in removal of uranium from aque-
wastewater was observed (Wilson and Edween, 1995). ous solution. The waste biomass of Sargassum sp. for the
Biosorption of Cu(II), Fe(II), Ni(II) and Zn(II) by non- recovery of ionic copper from simulated semiconductor
viable biomass of the cyanobacterium Phormidium lamino- effluents was investigated (Padilha et al., 2005) using con-
sum from single and binary metal solution was extremely tinuous system comprising of four column reactors filled
rapid and consisted of a single phase (Blanco et al., with the biomass which showed high operation stability
1998). The presence of a second metal in solution decreased and completely biosorbed the ionic copper from 63 l of
the binding of Fe(II), Ni(II) and Zn(II) due to chemical copper sulphate solution, 72 l of copper chloride solution
blocking of the carboxyl groups of biomass but this had and 72 l of copper nitrate solution, all the solutions con-
no effect on the binding of Cu(II). Washing with dilute taining 500 mg l 1 copper. Copper concentration was
acids was much faster and effective than NaOH, NaCl, found to be less than 0.5 mg l 1 in the effluent from the
CaCl2 and ultra pure water reaching equilibrium within outlet of the reactor. Five different brown seaweeds, Bifur-
30 min and the efficiency was independent of the concentra- caria bifurcata, Saccorhiza polyschides, Ascophyllum nodo-
tion of desorbent. Biosorption of Cu(II), Ni(II) and Cr(VI) sum, Laminaria ochroleuca and Pelvetia caniculata were
from aqueous solution by dried algae Chlorella vulgaris, studied for their ability to remove cadmium from aqueous
Scenedesmus obliquus and Synechocystis sp. was tested solution (Lodeiro et al., 2005). Kinetics of cadmium
under laboratory conditions as a function of pH, initial adsorption by all algae was relatively fast with 90% of total
metal ion and biomass concentration (Donmez et al., adsorption occurring in less than 1 h.
1999). Results showed the influence of algal biomass
concentration on metal uptake by all species and both Fre- 6.3. Removal of metals by bacterial biomass
undlich and Langmuir adsorption models described the
short-term biosorption. Out of 48 different species of red, Bacteria may uptake and accumulate a significant
brown and green algae examined for chromate adsorption, amount of metal ions, resulting in the transfer of metals
excellent adsorption was observed by Pachymeniopsis sp., to a contaminated matrix of biomass (Smith et al., 1994).
which had high selectivity for chromate among other heavy When suspension of dead biomass of actinomycetes from
metals ions such as cadmium and manganese. It also exhib- industrial fermentation, was mixed with wastewater, the
ited a typical Langmuir isotherm with qmax of 225 mg g 1 biosorption of cadmium cations occurred due to negatively
and K 1106 mg ml 1 (Lee et al., 2000). Biosorption of tri- charged sites on bacterial cell wall (Butter et al., 1996). Zinc
valent chromium by protonated brown algal biomass of biosorption capacity of Streptomyces rimosus biomass was
Eklonia revealed three types of functional groups. The car- studied in batch mode and after heat treatment (Mameri
boxyl group was the chromium-binding site within the pH et al., 1999). The optimum conditions of biosorption were
range of 1–5 at which chromium does not precipitate. The a contact time of 4 h, biomass particle size 140–250 lm,
pK value and number of carboxyl groups were estimated to ambient temperature, a stirring speed of 250 rpm and pH
be 4.6 ± 0.1 and 2.2 ± 0.1 mmol g 1, respectively (Yun 7.5. The biosorption capacity was 30 mg of Zn g 1 of
et al., 2001). Adsorption of Cu(II) from aqueous solution biomass, which increased up to 80 mg following chemical
by Ulothrix zonata was studied using batch adsorption treatment by NaOH. The removal of chromium, cadmium
technique (Nuhoglu et al., 2002). The equilibrium biosorp- and copper from dilute aqueous solution using dead
2252 S.S. Ahluwalia, D. Goyal / Bioresource Technology 98 (2007) 2243–2257

polysaccharide producing Ochrobactrum anthropi, isolated gated. The amount of Cr(VI) adsorbed increased with
from activated sludge (Ozdemir et al., 2003). Optimum increase in dose of these adsorbents and their contact time.
adsorption pH values of Cr(VI), Cd(II) and Cu(II) were Reduction rate of Cr(VI) to Cr(III) by Ecklonia sp. bio-
2.0, 8.0 and 3.0, respectively. Experimental showed the mass increased with decreasing pH, which appeared in the
influence of initial metal concentration on the metal uptake solution phase or was partly bound to the biomass (Park
for dried biomass. Both the Langmuir and Freundlich et al., 2004). The jack fruit peel (Artocarpus heterophyllus)
adsorption were suitable for describing the short term was treated with sulphuric acid to produce a carbonaceous
biosorption of Cr(VI), Cd(II) and Cu(II) by O. anthropi. product, which was used as an adsorbent for the removal
of Cd(II) from aqueous solution (Inbaraj and Sulochana,
6.4. Removal of metals by plant derived biomass 2004). Kinetic analysis made with Lagergren pseudo-first
order, Ritchie second order and modified Ritchie second
The sorption capacity of different biosorbents like dried order models showed better fits with modified Ritchie
mycelium of some species of fungi, baggase, rice husk and second order model. The Langmuir–Freundlich (Sips
fermented baggase was examined to remove cyanide from equations) model best defines the experimental equilibrium
industrial effluent (Azab et al., 1995). Banana pith (Musacea data among the three isotherm models (Freundlich, Lang-
zingiberales) was evaluated for its ability to sorb metal ions muir and Langmuir–Freundlich) used. A complete recov-
from electroplating waste and synthetic solutions under ery of the adsorbed metals ions from the spent adsorbent
both batch and continuous flow conditions. The sorption was achieved by using 0.01 M HCl.
was observed to be both pH and concentration dependent The adsorption of activated carbon prepared from apri-
with pH 4–5 being optimum. The equilibrium data followed cot stones, to remove Ni(II), Co(II), Cd(II), Cu(II), Pb(II),
the Langmuir isotherm model with maximum capacity of Cr(III) and Cr(VI) ions from the aqueous solution was
8.55 and 13.46 mg g 1 of Cu in electroplating waste and studied (Kobya et al., 2005). Highest adsorption occurred
synthetic solution, respectively (Low et al., 1995). at pH 1–2 for Cr(VI) and at pH 3–6 for the remaining
Waste biomass such as wheat stem and babul bark was metal ions. Further, adsorption capacities for these metals
used to remove nickel from effluent of an electroplating were found to in the order of Cr(VI) > Cd(II) > Co(II) >
industry (Verma and Shukla, 2000). The removal of nickel Cr(III) > Ni(II) > Cu(II) > Pb(II), respectively. Potential
was 2–10% less as compared to synthetic solution under of modified lignocellulosic fibre/jute was assessed for
similar conditions. Wheat straw activated carbon could adsorption of heavy metal ions like Cu(II), Ni(II) and
remove 100% Ni(II) from initial nickel concentration of Zn(II) from aqueous solution (Shukla and Pai, 2005).
25 mg l 1 at pH 4.0 in 4 h at 36 ± 2 C. The uptake capa- The dye loaded jute fibre showed adsorption capacity of
city of different metals by Quercus ilex phytomass (root, 8.4, 5.26 and 5.95 mg g 1 for Cu(II), Ni(II) and Zn(II),
stem and leaf) was found to be in the order of roots respectively, whereas oxidized jute fibre showed 7.73, 5.57
Ni > Cd > Pb > Cu > Cr; stem Ni > Pb > Cu > Cd > Cr; and 8.02 mg g 1 against 4.23, 3.37 and 3.55 mg g 1 for
and leaf Ni > Cd > Cu > Pb > Cr (Prasad and Freitas, unmodified jute fibre which followed Langmuir adsorption
2000). Desorption with 10 mM Na4 EDTA was effective model. Desorption efficiency, regenerative and reuse capa-
and there existed the possibility of recycling the phytomass. city of these adsorbent were also assessed for three succes-
Biosorption capacity of plant biomass of Indian Sarapa- sive adsorption–desorption cycles. The sorption of lead by
rilla (Hemidesmus indicus) was studied with toxic heavy tree fern, an agricultural by product was carried out using
metals like As, Se, Zn, Fe, Ni, Co, Pb, Mn, Hg, Cr and agitated and baffled system (Ho, 2005). The optimum pH
Cu. Lead was preferentially removed followed by Cr and for lead removal was 4.9. Also pseudo-second-order kinet-
Zn at concentration less than 250 mg l 1 and with biomass ics analysis was performed to determine the rate constant
quantity above 2 g. Presence of co-ions (As, Se and Hg) did of sorption, the equilibrium sorption capacity, and the ini-
not effect the Pb removal but Zn and Cr uptake decreased. tial sorption rate. Removal of cadmium from aqueous
Metal loaded biomass was regenerated with HNO3 and solution by Moringa oleifera seed was studied in batch
reused for three cycles without any loss in metal retention sorption experiments as a function of biomass dosage,
capacity (Chandrasekhar et al., 2003). Adsorption of contact time, metal concentration, particle size and pH
Cd(II) and Ni(II) was found to be higher than Cr(VI) (Sharma et al., 2006). Fourier transform infrared spectro-
and Zn(II) when phosphate treated rice husk was used as scopy indicated the amino-Cd interaction responsible for
an adsorbent (Ajmal et al., 2003). Sorption of Cd(II) was this sorption. These finding opens up new avenues in the
dependent on contact time, concentration, temperature, removal of toxic metals by shelled M. oleifera seeds from
adsorbent doses and pH of the solution and follows the water bodies as low cost, domestic and environment
Langmuir constant. Recovery of Cd(II) from aqueous solu- friendly safe technology.
tion by column operation was found to be higher than
batch process. Adsorption of Cr(VI) with activated rice 7. Development of biosorbent
husk carbon and activated alumina (Bishnoi et al., 2004)
and with formaldehyde treated saw dust and sulphuric acid Biosorption is a complex process, mainly comprising of
treated saw dust carbon (Garg et al., 2004) was investi- ion exchange, chelation and adsorption by physical forces
S.S. Ahluwalia, D. Goyal / Bioresource Technology 98 (2007) 2243–2257 2253

and entrapment in inter and intra-fibrillar capillaries and range of 5.0–13.5 mg g 1 under different operating condi-
space of the structural polysaccharide network as a result tions. The biosorption capacity of copper, cadmium and
of the concentration gradient and diffusion. There are sev- zinc on dried activated sludge was 0.32 m mol g 1 for metal
eral chemical groups that would attract and sequester the systems such as Cu–Cd; 0.29 m mol g 1 for Cu–Zn and
metals in biomass. Acetamide groups of chitin, structural 0.32 m mol g 1 for Cd–Zn. Results showed that biomass
polysaccharides of fungi, amino and phosphate groups of had a preference for copper followed by cadmium and zinc
nucleic acids, amide, amine, sulfhydryl and carboxyl (Hammaini et al., 2003). Another inexpensive source of
groups in the proteins and hydroxyls in polysaccharide of biomass is seaweeds comprising mainly the marine
marine algae belonging to Phaeophyceae, Rhodophyceae macro-algae. However, most of the studies on the up-
and Chlorophyceae are some of the examples. It does not take of toxic metals by marine algae and to some extent
necessarily mean that presence of functional groups guar- by freshwater algae are focused on toxicological aspects,
antees biosorption, perhaps due to steric, conformational metal accumulation and pollution indicators. There has
or other effects. been no focus on the technological aspects of metal
Several proprietory biosorption processes were devel- removal by algal biomass.
oped and commercialized in the early 1990s using Alga-
SORBTM (Brierley et al., 1986) and AMT-BioclaimTM 8. Conclusion
(Darnall, 1991) but did not attract widespread adoption
due to a lack of understanding of the underlying mech- Metabolic independent processes can mediate the bio-
anism of metal-sorption, proper selection of industrial logical uptake of heavy metal cations. Biosorption offers
effluents for pilot testing and scaling up of the process an economically feasible technology for efficient removal
(Kratochvil and Volesky, 1998). Routinely most prospec- and recovery of metal(s) from aqueous solution. The pro-
tive biosorbents are discovered by trial and experimenta- cess of biosorption has many attractive features including
tion. Many microorganisms can be used as biosorbents. the selective removal of metals over a broad range of pH
Fungi in particular have unique metal adsorption charac- and temperature, its rapid kinetics of adsorption and
teristics and are easy to cultivate (Gadd, 1988). They can desorption and low capital and operation cost. Biosorbent
successfully absorb toxic metal ions Zn2+, Cu2+, Cd2+, can easily be produced using inexpensive growth media or
Pb2+, Ni2+, Fe2+, Mn2+ and Cr6+ from aqueous solution. obtained as a by-product from industry. It is desirable to
But the process is susceptible to complexation or precipita- develop biosorbents with a wide range of metal affinities
tion of the metal, making it unavailable for binding due to that can remove a variety of metal cations. These will be
the presence of anions such as phosphate. Some biosorbent particularly useful for industrial effluents, which carry
have broad range, which bind the majority of heavy metals more than one type of metals. Alternatively a mixture of
with no specific activity, while others are specific for certain non-living biomass consisting of more than one type of
metals. Biosorption studies have been carried out using microorganisms can be employed as biosorbents. Such
easily available biomass in their native state or after simple ‘‘Combo’’ biosorbents have to be tested for commercial
processing. Among a variety of biomaterials, the majority applications. The use of immobilized biomass rather than
has been focused on bio-waste generated as a by-product native biomass has been recommended for large-scale
of large-scale industrial fermentation (Puranik and Pak- application but various immobilization techniques have
nikar, 1999), olive mill solid residues (Pagnanelli et al., yet to be thoroughly investigated for ease, efficacy and cost
2002), activated sludge from sewage treatment plants effectivity.
(Hammaini et al., 2003; Sag et al., 2003), biosolids (Norton Biosorption processes are applicable to effluents con-
et al., 2003), aquatic macrophytes (Keskinkan et al., 2003) taining low concentrations of heavy metals for an extended
and other plant derived materials (Gardea-Torresdey et al., period. This aspect makes it even more attractive for treat-
2004a,b). ment of dilute effluent that originates either from an indus-
Norton et al. (2003) used dewatered activated sludge trial plant or from the primary wastewater treatment
from a sewage treatment plant for removing zinc from facility. Thus biomass-based technologies need not neces-
aqueous solution and recorded adsorption capacity of sarily replace the conventional treatment routes but may
0.56 mM g 1 of biosolids. Use of biosolids for zinc adsorp- complement them. At present, information on different
tion was favorable compared to the bio-adsorption rate of biosorbent materials is inadequate to accurately define
0.3 mmol g 1 by seaweed Durvillea potatorum (Aderhold the parameters for process scale up and design perfection
et al., 1996). Keskinkan et al. (2003) studied adsorption including reliability and economic feasibility. To provide
characteristics of copper, zinc and lead on submerged an economically viable treatment, the appropriate choice
aquatic plant, Myriophyllum spicatum and found the of biomass and proper operational conditions has to be
adsorption capacities to be 46.60 mg l 1 for lead, identified. To predict the difference between the uptake
15.59 mg g 1 for zinc and 10.37 mg g 1 for copper. Pagna- capacities of the biomass, the experimental results should
nelli et al. (2002) carried out a preliminary study on the use be tested against an adsorption model. The development
of olive mill residue as a heavy metal sorbent material. of a packed bed or fluidized-bed biosorption model would
They found that copper was maximally adsorbed in the be helpful for evaluating industrial-scale biosorption
2254 S.S. Ahluwalia, D. Goyal / Bioresource Technology 98 (2007) 2243–2257

column performance, based on laboratory scale experi- Bai, S.R., Abraham, T.E., 2001. Biosorption of Cr(VI) from aqueous
ments and to understand the basic mechanism involved solution by Rhizopus nigricans. Bioresource Technology 79, 73–81.
Baik, W.Y., Bae, J.H., Cho, K.M., Hartmeier, W., 2002. Biosorption of
in order to develop better and effective biosorbent. heavy metals using whole mold mycelia and parts thereof. Bioresource
Critical analysis reveals that not all metal-polluted Technology 81, 167–170.
wastewater-generating industries have the interest or the Baillet, F., Magnin, J.-P., Cheruy, A., Ozil, P., 1998. Chromium
capability to treat effluents and most of the industries opt precipitation by the acidophilic bacterium Thiobacillus ferrooxidans.
only for basic treatment techniques simply to comply with Biotechnology Letters 20 (1), 95–99.
Bayramoglu, G., Bektas, S., Arica, M.Y., 2003. Biosorption of heavy
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convert the recovered metal into usable form. This will fur- Beveridge, T.J., Murray, R.G.E., 1980. Sites of metal deposition in the cell
walls of Bacillus subtilis. Journal of Biotechnology 141, 876–887.
ther require an interdisciplinary approach with integration Bishnoi, N.R., Bajaj, M., Sharma, N., Gupta, A., 2004. Adsorption of
of metallurgical skills along with sorption and wastewater Cr(VI) on activated rice husk carbon and activated alumina. Biore-
treatment to apply biosorption technology for combating source Technology 91, 305–307.
heavy metal pollution in aqueous system. Blanco, A., Sanz, B., Llama, M.J., Serra, J.L., 1998. Reutilization of non-
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