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A Review of The Biochemistry of Heavy Metal Biosorption by Algae and Its PS PDF
A Review of The Biochemistry of Heavy Metal Biosorption by Algae and Its PS PDF
A Review of The Biochemistry of Heavy Metal Biosorption by Algae and Its PS PDF
Review
A review of the biochemistry of heavy metal
biosorption by brown algae
Thomas A. Davisa,b, Bohumil Voleskya, Alfonso Muccib,*
a
Department of Chemical Engineering, McGill University, 3610 University Street, Montreal, Que., Canada H3A 2B2
b
Department of Earth and Planetary Sciences, McGill University, 3450 University Street, Montreal, Que., Canada H3A 2A7
Received 3 April 2002; received in revised form 25 April 2003; accepted 6 May 2003
Abstract
The passive removal of toxic heavy metals such as Cd2+, Cu2+, Zn2+, Pb2+, Cr3+, and Hg2+ by inexpensive
biomaterials, termed biosorption, requires that the substrate displays high metal uptake and selectivity, as well as
suitable mechanical properties for applied remediation scenarios. In recent years, many low-cost sorbents have been
investigated, but the brown algae have since proven to be the most effective and promising substrates. It is their basic
biochemical constitution that is responsible for this enhanced performance among biomaterials. More specically, it is
the properties of cell wall constituents, such as alginate and fucoidan, which are chiey responsible for heavy metal
chelation. In this comprehensive review, the emphasis is on outlining the biochemical properties of the brown algae that
set them apart from other algal biosorbents. A detailed description of the macromolecular conformation of the alginate
biopolymer is offered in order to explain the heavy metal selectivity displayed by the brown algae. The role of cellular
structure, storage polysaccharides, cell wall and extracellular polysaccharides is evaluated in terms of their potential for
metal sequestration. Binding mechanisms are discussed, including the key functional groups involved and the ion-
exchange process. Quantication of metalbiomass interactions is fundamental to the evaluation of potential
implementation strategies, hence sorption isotherms, ion-exchange constants, as well as models used to characterize
algal biosorption are reviewed. The sorption behavior (i.e., capacity, afnity) of brown algae with various heavy metals
is summarized and their relative performance is evaluated.
r 2003 Published by Elsevier Science Ltd.
Contents
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4312
2. Characteristics of the brown algae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4312
2.1. A comparison with other algae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4312
2.2. The brown algae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4314
3. Cellular structure and biochemistry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4314
3.1. Cellular structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4314
3.2. Storage polysaccharides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4315
certain multicellular algae, the gametes may be produced algae), laminaran is the main storage product, whereas
in special unicellular containers or gametangia; or (3) in the Rhodophyta (red algae) is distinguished by the
others, the gametangia are multicellular, whereby every oridean starch it produces and stores. Flagella are
gametangial cell is fertile and produces a gamete. absent in the Rhodophyta but they are found in
These characteristics are absent in vascular plants and the Chlorophyta and Phaeophyta.
form the basis by which the algae are studied and Of greater importance to the biosorption mechan-
classied. ism(s), however, is the presence and chemistry of the cell
Several characteristics are used to classify algae, wall. Biosorption in algae has mainly been attributed to
including the nature of the chlorophyll(s), the cell wall the cell wall properties where both electrostatic attrac-
chemistry, and agellation. One common characteristic tion and complexation can play a role. Cryptophyta, for
is that all types of algae contain chlorophyll a. However, example, does not have a cell wall [5]. Pyrrhophyta
the presence of phytopigments other than chlorophyll a (dinoagellates) can be naked or protected by
is characteristic of a particular algal division. The nature cellulosic thecal plates [4,5]. The Chrysophyceae of
of the reserve polymer synthesized as a result of the division Chrysophyta can be either naked or have
photosynthesis is also a key variable used in algal scales, cellulosic walls or a cell envelope [5]. None of
classication. It is important to point out, however, that these types of algae perform very well as heavy metal
there have been many classication schemes employed biosorbents.
to date and the following discussion is based on the Typical algal cell walls of Phaeophyta, Rhodophyta,
work of Bold and Wynne [4]. Accordingly, their and many Chlorophyta are comprised of a brillar
divisions include Cyanophyta, Prochlorophyta, Phaeo- skeleton and an amorphous embedding matrix. The
phyta, Chlorophyta, Charophyta, Euglenophyta, Chry- most common brillar skeleton material is cellulose
sophyta, Pyrrhophyta, Cryptophyta and Rhodophyta. (Fig. 1). It can be replaced by xylan in the Chlorophyta
Table 1 is a summary of algal divisions, restricted to and Rhodophyta in addition to mannan in the
those which possess a cell wall, and their most signicant Chlorophyta. The Phaeophyta algal embedding matrix
characteristics. When comparing Phaeophyta (brown is predominately alginic acid or alginate (the salt of
algae) to other common algal divisions such as the alginic acid; Fig. 7) with a smaller amount of sulfated
Chlorophyta (green algae), important differences are polysaccharide (fucoidan; Fig. 6) whereas the Rhodo-
seen in the storage products they utilize as well as in phyta contains a number of sulfated galactans (e.g. agar,
their cell wall chemistry. In the Phaeophyta (brown carregeenan, porphyran, etc.). Both the Phaeophyta and
Table 1
Three algal divisions and signicant characteristics
Chlorophyta Green algae Chlorophyll a,b; a-, Starch (amylose and Cellulose in many Present
b- and g-carotenes amylopectin) (oil in (b-1,4-gluco-
and several some) pyroside), hydroxy-
xanthophylls proline glucosides;
xylans and
mannans; or wall
absent; calcied in
some
Phaeophyta Brown algae Chlorophyll a,c; Laminaran (b-1,3- Cellulose, alginic Present
b-carotene and glucopyranoside, acid, and sulfated
fucoxanthin and predominantly); muco-
several other mannitol polysaccharides
xanthophylls (fucoidan)
Rhodophyta Red algae Chlorophyll a (d in Floridean starch Cellulose, xylans, Absent
some Florideo- (amylopectin-like) several sulfated
phyceae); R- and polysaccharides
C-phycocyanin, (galactans)
allophycocyanin; calcication in
R- and B-phyco- some; alginate in
erythrin. a- and b- corallinaceae
carotene and several
xanthophylls
Information in this table is from a similar, more extensive table compiled by Bold and Wynne [4].
ARTICLE IN PRESS
4314 T.A. Davis et al. / Water Research 37 (2003) 43114330
outside
inside
Fig. 1. Cell wall structure in the brown algae. After Schiewer and Volesky [2].
Rhodophyta divisions contain the largest amount of genuses and species studied for their heavy metal
amorphous embedding matrix polysaccharides. This binding ability. The boxes outline the orders and
characteristic, combined with their well known ability families of principal interest in biosorption.
to bind metals, makes them potentially excellent heavy
metal biosorbents.
3. Cellular structure and biochemistry
2.2. The brown algae
3.1. Cellular structure
The brown algae are an important assemblage of
plants that are classied in about 265 genera with more A typical brown algal cell is depicted in Fig. 3. The
than 1500 species [4]. They derive their characteristic chloroplast envelope (Ce) contains the chloroplasts
colour from the large amounts of the carotenoid which have three thylakoids (an interconnected set of
fucoxanthin (which yields a brown colour) contained in disc-like sacs) per band. This structure (known as a
their chloroplasts and the presence of various pheophy- plastid; the most common of which is the chloroplast)
cean tannins. They occur mainly in the marine environ- stores food material and contains chlorophyll a, c1, and
ment, where they appear as an intertidal component. c2. In addition to the chloroplast envelope, the
Some marine forms penetrate into brackish environ- chloroplasts are surrounded by the two membranes of
ments, and can be an important part of the salt marsh the chloroplast endoplasmic reticulum (Cer). The outer
fauna [5]. Brown algae ourish in temperate to subpolar membrane which encloses an inner membrane is
regions where they exhibit the greatest diversity in species discontinuous with the nuclear envelope (Ne) in Fucales
and morphological expression. and Laminaria although it is continuous as seen in Fig. 3
The division Phaeophyta is subdivided into orders, for the brown algal order Ectocarples [5].
which subsequently are divided into families, and then Although most of the algal cellular functions are
the familiar genus and specie are specied. There are 13 coded for by nuclear DNA, a few organellar proteins are
orders in the Phaeophyta according to the classication coded from within the chloroplast. These microbrils of
of Bold and Wynne [4]; however, from the point of view DNA (Fib) occur in the plastids. They can be either
of biosorption, only two are of importance, namely the linear or of closed circular form and are attached to the
orders Laminariales and Fucales (Fig. 2). Both orders thylakoid membranes [7]. As in all eukaryotes, DNA is
are abundant in nature and include the most structurally housed in the nucleolous (Nu) of the nucleus (N). The
complex algae. Laminariales are collectively referred to prenoid (P) is responsible for CO2 xation and
as kelps and are harvested for many commercial uses the formation of storage products. It is enclosed by the
(e.g. water holding property for frozen foods, syrups, prenoid sac (Ps) and extends out from the chloroplast
and frozen deserts; gelling property for instant puddings endoplasmic reticulum.
and dessert gels, or even explosives; emulsifying proper- Production and secretion of the polysaccharides take
ties for polishes; stabilizing properties in ceramics, place in the dictyosome (D), otherwise known as the
welding rods and cleaners) [6]. The order Fucales is a golgi apparatus or golgi dictyosome. The mitochondrian
large and diversied order, with a great amount of (M) is the site of cellular respiration where ATP is
morphological diversity [4]. For example, the family formed. Each mitochondrian is bounded by a double
Sargassaceae contained within it, is well known for the membrane which creates two different compartments
algal genus Sargassum which is found in the tropical within the organelle (organelle or little organ
waters of the Sargasso Sea. Fig. 2 outlines some of the describes the various internal structures of the cell, each
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T.A. Davis et al. / Water Research 37 (2003) 43114330 4315
Families
Families
Fig. 2. Classication scheme and important brown algae in the study of biosorption. Boxes enclose orders and families of principal
interest in biosorption. Classication is after that of Bold and Wynne [4].
growth in length, they can display a predominantly tenerium this value reaches between 30% and 35% [6].
longitudinal orientation. The mass fraction of cellulose The alginate of Sargassum fluitans has been reported [25]
may be 220% of the dry weight according to Kreger to account for 45% of its dry weight once it has
[17]. For example, the cellulose content of Ascophyllum been stripped of its sea salts and converted to the
and Laminaria (Fig. 2) were determined to be 7% and protonated form. Davis et al. [26] also reported similar
20%, respectively [21]. alginate yields for protonated Sargassum fluitans and
Sargassum oligocystum of approximately 45% and 37%,
3.3.1. Extracellular polysaccharides: fucoidan respectively.
Fucoidan has been found to occur in several members Alginic acid or alginate, the salt of alginic acid, is the
of the family Laminariaceae (Fig. 2), with dry mass common name given to a family of linear polysacchar-
percentages between 5 and 20 [22]. It also occurs ides containing 1,4-linked b-d-mannuronic (M) and a-l-
abundantly in species of Fucus and Chordaria, as well guluronic (G) acid residues arranged in a non-regular,
as other brown algae. The compound was rst isolated blockwise order along the chain ([27]; Fig. 7ac). The
by Kylin [23] who prepared and isolated l-fucose residues typically occur as (M)n, (G)n, and (MG)n
phenylhydrazone from the hydrolyzate [12]. sequences or blocks. The carboxylic acid dissociation
Fucoidan is a branched polysaccharide sulfate ester constants of M and G have been determined as pKa
with l-fucose 4-sulfate building blocks as the major 3:38 and pKa 3:65; respectively, with similar pKa
component (Fig. 6). They are predominantly a1-2- values for the polymers [28], where
linked [75]. Acid hydrolysis of fucoidan also yields
various amounts of d-xylose, d-galactose, and uronic pKa log Ka
acid [18]. and
COO H
3.3.2. Extracellular polysaccharides: alginic acid Ka :
COOH
Alginic acid occurs in all brown algae [12]. It may be
present in both the cell wall matrix and in the mucilage The salts of alginic acid with monovalent ions (alkali
or intercellular material (Figs. 1,7; [6,18]) and can metals and ammonium) are soluble, whereas those with
constitute between 10% and 40% of the dry weight divalent or polyvalent metal ions (except Mg2+) and the
(untreated) of the algae [12]. Its abundance is dependent acid itself are insoluble [12].
on the depth at which the algae are grown and it also M- and G-block sequences (see Fig. 7) display
displays seasonal variations. The latter may reect signicantly different structures and their proportions
changes associated with growth stages [24,17]. The in the alginate determine the physical properties and
alginic acid content in Sargassum longifolium was found reactivity of the polysaccharide [29]. Polymannuronic
to be 17%. For Sargassum wightii and Sargassum acid is a at ribbon-like chain; its molecular repeat is
H O
COO
H CH O O OH O OH
3 COO
H O OH HO OH HO
-O3SO H H HO H HO H
OH H H CH O -D-mannopyranuronate -L-gulopyranuronate
3 (M) (G)
H O (a)
-O3SO H H
OH H H CH O OOC OH OOC OH OOC
O O O HO
3 OH O
O
H HO O HO O OH
H O H O
OH
OOC HO O
O O
O OH H OH OOC OH
H CH
3
H O G G M M G
-O3SO H
H (b)
OH H
H CH O
3 GMMMMGGGGGGGMGMGMGMGMMMMG
H O
-O3SO H M-Block G-Block MG-Block M-Block
-O3SO H (c)
Fig. 6. The structure of fucoidan, a branched polysaccharide Fig. 7. Alginate structural data: (a) alginate monomers (M vs.
sulfate ester with l-fucose building blocks as the major G); (b) the alginate polymer; (c) chain sequences of the alginate
component with predominantly a1-2-linkages. polymer. After Smidsr^d and Draget [19].
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4318 T.A. Davis et al. / Water Research 37 (2003) 43114330
constitute the highest percentage of titratable sites such as HCl whereby the proton displaces the light metal
(typically greater than 70%) in dried brown algal ions from the binding sites (i.e. carboxylic, sulfonic, and
biomass. The adsorption capacity of the algae is directly others). In the second, the biomass is reacted with an
related to the presence of these sites on the alginate aqueous solution of a given ion at high concentration so
polymer, which itself comprises a signicant component that the majority of sites are occupied by, for example,
(up to 40% of the dry weight, [12]) of the dried seaweed calcium or potassium. In cases where the non-treated
biomass. Furthermore, the majority of metals of interest marine alga Sargassum was reacted with a (heavy)
(i.e. Cd2+, Co2+, Cu2+, Fe2+, Ni2+, Pb2+) display metal-bearing solution, a pH increase and the release of
maximal or near maximal sequestration at pHs near the light metal ions was observed. This also was explained in
apparent dissociation constant of carboxylic acids terms of ion-exchange, whereby the observed release of
observed in brown algal biomass (pK0 near 5). The role light metals balanced the uptake of protons and heavy
of carboxylic groups in the adsorption process has been metals. When the heavy metal concentration was
clearly demonstrated by a reduction in cadmium and increased, little pH increase was observed and this was
lead uptake by dried Sargassum biomass following attributed to the fact that the maximum binding
partial or complete esterication of the carboxylic sites capacity of the biomass had been reached and all
[25]. Finally, Fourier-transformed infrared (FTIR) exchangeable sites were occupied by the heavy metal
spectral analyses have shown that cadmium biosorption [42]. In related metal uptake experiments with treated
to Sargassum arises from bridging or bidentate (see biomass (protonated), the pH of Sargassum suspensions
below) complex formation with the carboxylate groups decreased. This was observed as either a continual but
of the alginate [25], consistent with the above described initially steep drop in pH in a free-drift system, or by the
egg-box model of Rees and co-workers [38,39]. addition of base in a pH-stat system. Again, this was
The second most abundant acidic functional group in interpreted as ion-exchange between protons and the
brown algae is the sulfonic acid of fucoidan. Sulfonic heavy metal ions at the binding sites [42].
acid groups typically play a secondary role, except when It should be pointed out that the term ion-exchange
metal binding takes place at low pH. Hydroxyl groups does not explicitly identify the binding mechanism,
are also present in all polysaccharides but they are less rather it is used here as an umbrella term to describe the
abundant and only become negatively charged at experimental observations. The precise binding mechan-
pH>10, thereby, also playing a secondary role in metal ism(s) may range from physical (i.e. electrostatic or
binding at low pH. Londonvan der Waals forces) to chemical binding (i.e.
ionic and covalent). The term sorption would refer to
4.2. Ion-exchange binding of a metal cation to a free site as opposed to one
that was previously occupied by another cation. It is
Ion-exchange is an important concept in biosorption, distinct from adsorption that, strictly speaking, denes
because it explains many of the observations made binding in terms of a physical rather than chemical
during heavy metal uptake experiments. Furthermore, it surface phenomenon. In the case of biosorption of heavy
is a natural extension to the premise that alginate plays a metals by brown algal biomass, the mechanisms can be
key role in biosorption by brown algae, since it has been viewed, in principle, as being extracellular, or occurring
shown that ion-exchange takes place between metals discretely at the cell wall. Intracellular sorption would
when binding to alginate [76]. Kuyucak and Volesky normally imply bioaccumulation by a viable organism.
[40,41] reported an enhanced release of ions (Ca2+, K+,
Mg2+, Na+) from the alga Ascophyllum nodosum when 4.3. Definitions
reacted with a cobalt bearing aqueous solution rather
than cobalt-free solution. Furthermore, when the alga The following denitions are based on the text by
was pre-treated with CaCl2 and HCl, a 2:3 stoichio- Stumm and Morgan [43]. Any combination of cations
metric relationship was observed between Ca2+ release with molecules or anions containing free electron pairs
and Co2+ uptake. Schiewer and Volesky [2] point out, (bases) is termed coordination, also known as complex
however, that a ratio closer to one would have been formation. Coordination or complex formation, in turn,
achieved if protons were included in the charge balance. may be either electrostatic (i.e. Coulombic) or covalent in
It was concluded that ion-exchange was the dominant character. The heavy metal cation that is bound is often
mechanism. designated as the central atom, and is distinguished from
Untreated biomass generally contains light metal ions the anions or molecules with which it forms a
such as K+, Na+, Ca2+, and Mg2+. These are coordination compound, the ligand(s). When the ligand
originally bound to the acid functional groups of the is composed of several atoms, the atom responsible for
alga and were acquired from seawater. Treated biomass the basic or nucleophilic nature of the ligand is termed
generally implies one of two chemical alterations. The the ligand atom. A base containing more than one
rst is protonation of the biomass with a strong acid ligand atom, a multidentate complex, may occupy more
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4320 T.A. Davis et al. / Water Research 37 (2003) 43114330
than one coordination position in the complex. Complex alginate. Regions of the alginate polymer rich in G
formation with multidentate ligands is termed chelation; residues (G-blocks), which display a higher selectivity
complexes are chelates. Furthermore, the coordination for divalent metal ions, provide a multi-dentate envir-
number refers to the number of ligand atoms surround- onment for complexation whereas in regions rich in
ing the central atom, where most metal cations engage in mannuronic acid complexation would be predominantly
coordinations of 2, 4, 6, and 8, with 4 and 6 being the monodentate and therefore weaker. In other words, the
most common. In the case of polymers these values may higher specicity of guluronic acid supports the hypoth-
be lower due to steric effects. A proton complex has a esis that the coordination number of the metal bound to
coordination number of one, as opposed to the higher guluronic acid residues is larger than with mannuronic
coordination numbers found in metal complexes [43]. acid residues. More specically, the key appears to be
Although this terminology is typically employed for the orientation of the oxygen atoms with respect to
aqueous complexation with small ligands, the terms are COO. In guluronic acid the ring oxygen and the axial
often applied in the literature when dealing with more O-1 form a spatially favorable environment with
complex molecules, thus this outline is intended to serve COO, as opposed to the equatorial O-1 which occurs
as a basis for its usage. in mannuronic acid residues (see Fig. 7).
The terms inner-sphere and outer-sphere complex are Much less work has been carried out on the metal
used to distinguish between binding which is, respec- binding ability of fucoidan. The afnity sequence has
tively, largely covalent in character or chiey electro- been reported [47] as Pb2+>Ba2+>Cd2+>Sr2+>
static in nature. In the rst case, the interacting ligand is Cu2+>Fe2+>Co2+>Zn2+>Mg2+>Cr3+>Ni2+>
immediately adjacent to the metal cation. In the second Hg2+>Ca2+.
case, ions of opposite charge are attracted and approach
each other within a critical distance and effectively form
what is termed an ion pair. In outer-sphere complexes, 5. Biosorption by brown algae
the metal ion or the ligand or both generally retain their
coordinated water when the complex is formed. In other 5.1. Quantifying metalbiomass interactions
words, the metal ion and the ligand are most often
separated by one or more water molecules [43]. 5.1.1. Sorption isotherms
From a scientists perspective, the eld of biosorption
4.4. Complexation is a challenging one, since it requires the application of
rst principles of organic chemistry and geochemistry.
The nature of complexation as it occurs within the The main objectives are the elucidation of binding
brown algae will be addressed by reviewing reported mechanisms, the relative afnity of heavy metals for the
observations in binding of heavy metals by alginate. biomass, and how both are affected by varying
Haug [28], in his study of metal-ion binding to alginic environmental conditions. Ultimately, the goal is the
acid extracted from Laminaria digitata, reported that the successful implementation of a remediation program.
amount of protons released into solution decreased The rst step towards these objectives is to quantify
in the order Pb2+>Cu2+>Cd2+>Ba2+>Sr2+> the capacity of a given biomass to sequester heavy
Ca2+>Co2+>Ni2+>Mn2+>Mg2+. He explained metals from an aqueous solution. This is traditionally
these results in terms of the relative ability of the done by characterizing the equilibrium state after the
binding metal to compete with protons for organic biomass (i.e. treated or untreated brown alga) has been
binding sites. The afnity sequence for metal-ion allowed to react with an aqueous solution of the metal of
binding to alginate extracted from L. digitata followed interest. The reaction is commonly monitored by
a similar trend: Cu2+>Ba2+>Ca2+>Co2+ [28]. The measuring the amount of metal remaining in solution
binding strength of alkaline earth metals to both until it becomes time invariant. The model used to
polymannuronate and polyguluronate was found to describe the results should be capable of predicting
decrease in the order Ba2+>Sr2+>Ca2+>Mg2+ [44]. heavy metal binding at both low and high concentra-
Haug and Smidsr^d interpreted the preferential binding tions. Ideally the model should not only be predictive
of heavier ions to stereochemical effects, since larger but should rest on our understanding of the mechanism
ions might better t a binding site with two distant of biosorption.
functional groups. The Langmuir adsorption isotherm has traditionally
The egg-box model, in addition to other models been used to quantify and contrast the performance of
with more accurate steric arrangements have been different biosorbents. However, in order to evaluate the
supported by X-ray diffraction [45] and NMR spectro- appropriateness of this model we must look at its
scopic analyses [46]. Accordingly, we can view metal underlying assumptions.
sequestration as the complexation (or coordination) of a The Langmuir isotherm was originally developed to
central heavy metal to a multidentate ligand, the describe the gassolid phase adsorption of activated
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T.A. Davis et al. / Water Research 37 (2003) 43114330 4321
carbon. In its formulation, binding to the surface was which has a different afnity for a sorbing heavy metal.
primarily by physical forces (i.e. electrostatic or Lon- Furthermore, the one-to-one stoichiometry is also not
donvan der Waals forces) and implicit in its derivation complied with, since ion-exchange has been shown to be
was the assumption that all sites possess equal afnity a dominant mechanism, and typically approximately
for the adsorbate. Its use was extended to empirically two protons are released upon the binding of one
describe equilibrium relationships between a bulk liquid divalent heavy metal ion. Despite this fact, the
phase and a solid phase. Langmuir equation is frequently used to t experimental
One of the simplest representations of the adsorption data (Fig. 10). In this case, the following form of the
phenomenon calls for the migration to and the occupa- Langmuir equation (Eq. (7)) is traditionally applied:
tion of a surface site, S, on a solid (adsorbent) by an
bCf
adsorbate, A. This can be represented by an equilibrium q qmax ; 8
1 bCf
reaction:
where q is the uptake (mmol heavy metal/gram
S A3SA; 1
biosorbent) and qmax is the maximal uptake (mmol
where SA is the adsorbed complex. Surface species heavy metal/gram biosorbent) of the biosorbent. Cf is
concentrations may be expressed as moles per liter of the nal equilibrium solution concentration of the
solution, per gram of solid, per unit area of solid surface heavy metal, which is typically determined by atomic
or per mole of solid. Assuming that all surface sites have
the same afnity for the solute A, a mass action law can
be written as EQUILIBRIUM SORPTION ISOTHERM
METAL
SA DGads LANGMUIR
Kads exp : 2 UPTAKE q = q max b C f model
SA RT [mg/g] 1 + b Cf
we obtain 0.8
Kads A
G Gmax : 7
1 Kads A 0.6
same energy or equal afnity for the adsorbate). A Final Concentration C f [mM Cd]
typical Langmuir adsorption isotherm is shown in
Fig. 10. Cadmium sorption isotherms for raw and unsorted (all
Fig. 9. size fractions) Sargassum species at pH=4.5: (&) S. poly-
At least one of these conditions is implicitly not met in cystum, Cebu, Philippines; (J) Sargassum, unidentied,
the case of biosorption. We have seen in the previous Australia; (m) S. filipendula, Brazil; (E) S. muticum, UK. Solid
sections that there is more than one type of functional curves are calculated with the Langmuir equation. After Davis
group contributing to the biosorption process, each of et al. [54].
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4322 T.A. Davis et al. / Water Research 37 (2003) 43114330
the solution and on the biosorbent (S. fluitans). acid as sorption proceeded. Base was added in
Furthermore, the model was capable of tting and most cases since the biomass was generally pre-treated
predicting biosorption isotherms for different pH values with acid, effectively removing the associated light
as well as the equilibrium uranium desorption concen- metal ions. Protonated acid functional groups therefore
trations. exchange for the binding metals and release H+ to
Schiewer and Volesky [42,52,53] presented a series of the solution. The purpose of maintaining pH is to
equilibrium biosorption models which incorporate the optimize total metal uptake. The salts of the various
metal-ion concentration, pH and ionic strength. One of heavy metals used for these experiments as well as
the proposed models utilizes one tting parameter in discussions on the various forms and binding mechan-
which the formation of BM0.5 complexes was assumed. isms of the metals can be found in the corresponding
They employed a combined Donnan-biosorption-iso- references.
therm equation that allowed for direct calculation of
cation binding without interactions when swelling 5.2. Alginate conformation: influence on selectivity of the
proportional to the number of free sites was assumed. raw biomass
The Donnan model considers that the intraparticle
concentration of ionic species may be different from In accordance with the concept that metal binding to
the bulk concentration and, therefore, swelling becomes brown algal biomass can be approximated by the ion-
an important parameter since the biomass (Sargassum exchange process, as was indicated earlier in the text, we
fluitans in these experiments) swells with increasing will now extend the discussion to incorporate the
pH (albeit to a lesser extent in the presence of inuence of the macromolecular conformation of
divalent cations). Using the parameters (number of alginate on the metal selectivity as it pertains to applied
binding sites, proton binding constant, and specic biosorption. To this end, recent advances in the
particle volume) obtained from pH titrations, it was characterization of biopolymer conformational varia-
possible to predict the effect of Ca concentration, pH bility have allowed us to demonstrate the importance
and ionic strength on the binding of Ca for a brown of the biochemical composition of the raw biomass
algal biosorbent. in determining heavy metal selectivity (e.g. metal
binding afnity sequence, selectivity of the raw biomass,
5.1.4. Biosorption of different heavy metals by brown and the inuence of ionic strength on binding in
algae multiple-metal systems). By documenting the variability
There has been an intense research effort aimed at of alginate conformation that exists naturally among
characterizing the metal binding properties of various samples of raw biomass, we will be able to correlate
forms of biomass. These have included fresh and salt parameters such as alginate co-polymer block structure
water algae, bacteria, fungi and yeasts. Metal sequestra- to metal binding behavior in ow-through remediation
tion by this diverse group of biosorbents was summar- systems.
ized by Volesky and Holan [1] and serves as a good
comparison to the biosorptive behavior of marine 5.2.1. Conformational variability of alginates derived
brown algae. Uptake of metals by different brown algae from Sargassum spp.
is summarized in Table 3. It has been reported [58] that most Sargassum
The algae most frequently studied were Ascophyllum alginates have M:G ratios ranging from 0.8 to 1.5,
nodosum, Fucus vesiculosus, Laminaria japonica, and whereas alginates from species such as A. nodosum
various species of the genus Sargassum. (B1.2; Order Fucales) and L. japonica (B2.2; Order
As shown in Table 3, the metal uptake in mmol/g Laminariales) possess relatively high M:G ratios
biomass typically does not exceed approximately [6,33,34,36,59,60]. As will be discussed in more detail
2 mmol/g. The values were tabulated from experimental below and, as indicated in preceding sections of this
data acquired at sufciently high initial metal concen- review, low M:G ratios (i.e. o1.0) are indicative of
trations so that maximal uptake (corresponding to the higher G content and are, therefore, deemed highly
qmax of the Langmuir isotherm) was achieved. The only advantageous for the implementation of the biosorption
exception is for Au uptake (2.03 mmol/g) by Sargassum process. This reects the established selectivity for
natans where the experiments do not appear to have divalent cations of the guluronic block sections, in
been run at sufciently high gold concentrations. It accordance with the egg-box model of Rees and co-
can also be seen that the pH at which the maxima workers.
were achieved is not the same for all heavy metals, as Recent studies on the macromolecular conformation
would be expected on the basis of the varying afnity of [26,61] of Na-alginates extracted from various species of
the metals for the acidic functional groups (i.e. Sargassum reveal a consistent and unusual enrichment
carboxylic and sulfonic). The pH was held constant in in homopolymeric a-l-guluronic acid (G-blocks).
each case by, typically, adding small amounts of base or Table 4 lists the monomer and diad guluronic acid
ARTICLE IN PRESS
4324 T.A. Davis et al. / Water Research 37 (2003) 43114330
Table 3
Uptake of metals by different brown algae
UO2+
2 Sargassum fluitans 4.0 1.59 Yang and Volesky [57]
frequencies (FG ; FGG ) and the M:G ratios measured for Table 4
several of these extracts. Davis et al. [61] demonstrated Compositional data of Na-alginates extracted from species of
that for these Na-alginates, the frequency of diad pairs Sargassum
approximated the frequency of homopolymeric guluro- Source of alginate FG FGG M:G ratio
nic acid triads (GGG or FGGG ). Accordingly, it is a
possible to use the frequency, FGG ; to quantify the S. fluitans 0.84 0.81 0.19
degree of guluronic acid homopolymeric block forma- S. siliquosuma 0.58 0.57 0.72
S. filipendulab 0.84 0.76 0.19
tion (e.g. a low M:G ratio does not explicitly indicate a
S. muticumb 0.76 0.59 0.31
high G-block frequency). As such, the results presented S. polycystumb 0.82 0.77 0.21
in Table 4 clearly indicate that these alginates are highly
a
enriched in G-blocks when compared to the vast Davis et al. [61].
b
majority of alginates extracted from other brown algae Davis et al. [26].
[32,62,85]. Similar compositions, among other brown
algae, are only known to occur in the stipes of Laminaria alginates may provide additional advantages for the use
hyperborea, which typically yield a FGG on the order of of these brown algae in implementation scenarios (see
0.4. The metal selectivity imparted by these G-block rich below).
ARTICLE IN PRESS
T.A. Davis et al. / Water Research 37 (2003) 43114330 4325
5.2.2. Selectivity studies relevant to the biosorption higher than the Na-alginates employed by Jang et al.
process [66].
In the section on alginate metal afnity and binding, The relationship between alginate conformation in
we reviewed some of the earlier work (e.g. [35]) that Sargassum species and metal selectivity has recently been
demonstrated the selective binding of divalent cations by established [26] for the CaCd, CaMg and CdMg
alginates containing signicant levels of guluronic acid. alginate systems. In that study, the selectivity coefcient
These early investigations were followed by studies of for the ion-exchange of two cations, A and B, is dened
mixed-metal pair systems, in which both the extracted by the following reaction and equilibrium relationship,
alginate and the raw biomass were compared on the and was determined according to the method of Haug
basis of their selectivity coefcients. Haug and Smidsr^d and Smidsr^d [35,63]:
[87] demonstrated that selectivity coefcients of ex-
S Ag Baq "
S Bg Aaq ; 13
tracted alginates for the strontiumcalcium and stron-
tiummagnesium metal pair systems are closely
K BA XB CA =XA CB ; 14
correlated to coefcients obtained with the raw brown
algal tissue. In both cases, there was an enhanced where (g) is the gel or alginate phase; (aq) the aqueous
selectivity for strontium over magnesium or calcium as phase; S the binding site; XA and XB the equivalent
the guluronic acid content of the alginate in the algal fractions of the counterions in the polymer phase,
tissue increased. The experiments performed by Haugs whereby XA XB 1; and CA and CB are the
group were typically carried out at a relatively high ionic concentrations of the same ions in solution. The
strength (on the order of 0.2 M) but the selectivity selectivity coefcients for the CdCaalginate system,
coefcients determined in their studies still reect the K CaCd ; varied from between 0.4370.10 and 1.3270.02
relative afnity of the alginates and raw biomass at for a range in FGG of 0.230.81. In contrast, the
environmentally relevant metal concentrations. MgCa and MgCdalginate systems yielded maximal
A signicant amount of work was published on the values of K Ca Cd
Mg (18.071.4) and K Mg (16.070.9) for the
binding of Cu2+ to alginate by Jang et al. [6466]. In alginates extracted from Sargassum fluitans
particular, they demonstrated the usefulness of the (FGG 0:81) and Sargassum thunbergii (FGG 0:75).
selective nature of Na-alginate gels in the eld of heavy The lack of signicant selectivity between Ca2+ and
metal remediation. For example, Jang et al. [66] Cd2+ for a wide range of FGG may reect the
performed competitive uptake experiments between importance of steric placement in the alginate gel
Cu2+ and Co2+ by a Na-alginate gel at intermediate network, since the two cations have similar ionic radii
(100 ppm or B1.6 mM) as well as low Cu (18 ppm or (1.00 and 0.95 A,( for a 6-fold coordination, respectively).
0.28 mM) and high Co2+ (300 ppm or 5.1 mM) con- The high selectivity coefcients observed for the
centrations which revealed a high selectivity for Cu2+ CaMg and CdMgalginate systems may, in part, be
over Co2+ (Cu/Co selectivity=20.9, based on batch ascribed to the difference between the ionic radius of
adsorption and an extended Langmuir model). In both Mg2+ (0.72 A, ( for a 6-fold coordination) and that of
cases more than 90% of the Cu2+ was sequestered either Ca2+ or Cd2+. Hence, the size of the cation appears
preferentially over Co2+ from the solution. The Na- to be an important variable in metal binding to alginates,
alginate (CP Kelco; likely extracted from M. pyrifera or both due to the rigid nature of the GG-linkages, as well as
L. hyperborea) was characterized and found to contain to the steric arrangement of the electronegative ions
only 31% guluronic acid (FG 0:31), and the authors surrounding the divalent cation. In contrast to Ca2+ and
acknowledged that an even greater selectivity for Cu2+ Cd2+, the lower selectivity of magnesium for the G-blocks
over Co2+ could be expected for Na-alginates contain- likely results from its inability to form as tight a
ing higher amounts of guluronic acid residues. On the coordination environment within the alginate network.
basis of these observations and those of Haug and All of the above observations can be related to the
Smidsr^d [87,35], raw brown algal tissues that contain original observations of Haug and Smidsr^d [35], who
guluronic acid-rich alginates should display a high metal determined the amount of various divalent metal cations
selectivity. This conclusion is supported by the work of required to bring about gel-formation and precipitation
Figueira et al. [56] in which they investigated the of alginates extracted from Laminaria digitata and the
interference of Fe2+ on Cd2+ biosorption by raw stipes of Laminaria hyperborea. The relative amount of
Sargassum biomass. They documented a marked selec- each metal ion required for gelation does not correspond
tivity for Cd2+ over Fe2+ at concentrations ranging exactly with the afnity sequence of the individual
from 0.1 to 10 mM Cd2+. The authors did not specify metals for the alginate (see Complexation) but accurately
the guluronic acid composition of the alginates con- reects the relative selectivity of alginate in mixed-metal
tained within the thallus of their Sargassum but the data systems. The discrepancies are attributed to the differ-
of Davis et al. [26,61] indicate that the frequency of ence in the absolute quantity of a given metal ion
guluronic acid diads (FGG ) of Sargassum are likely required to obtain a gel. The amount of divalent metal
ARTICLE IN PRESS
4326 T.A. Davis et al. / Water Research 37 (2003) 43114330
ions required for precipitation of the alginate increases generated. According to this scenario, the biosorbent is
from right to left and, thus, their relative selectivity regenerated and a highly concentrated metal solution is
increases to the right: obtained. This concentrate may then be treated by either
co-precipitation, occulation or electro-winning. A toxic
Mg > Mn; Fe > Co > Ni > Zn > Ca > Cd > sludge would be generated by co-precipitation whereas
Sr > Cu > Pb > Ba: the solid metal, a more desirable end-product, would be
recovered from the concentrate by electro-winning. A
For example, measured selectivity coefcients in both simplied schematic representation of the proposed
alginate gels and raw brown algal tissue correspond to zero discharge technology is shown in Fig. 11 where
the above sequence for the following metal-pair systems: multiple sorption and desorption cycles are carried
Sr>Mg; Sr>Ca; Cu>Co; Cd>Fe; CdBCa; Ca>Mg out.
and Cd>Mg. Although these experiments were per- The application of biosorption is particularly well
formed with different alginates and raw algal thalli, a suited as a rening technique where wastewater heavy
common property of all these substrates was the metal concentrations range from 1 to 100 ppm. These
presence of a minimum frequency of guluronic acid levels can be lowered to drinking water standards with
residues (i.e. FG > B0:30). An exact comparison is the existing biosoption technology. The main advan-
therefore not possible, but the evidence of selective tages of the biosorption process over traditional
binding obtained through the variety of experiments techniques are the high efuent quality it generates, its
outlined in this review (e.g. selectivity experiments, terms of operation under a broad range of service
batch metal uptake experiments) clearly lends credibility conditions and its cost-effectiveness. The bottom line is
to the application of the egg-box model in explaining the inexpensive nature of brown algal biosorbents.
the metal selectivity displayed by brown algal
biosorbents. 5.4. Relating alginate conformation and metal selectivity
to applied biosorption
5.3. Potential for applied remediation
It is beyond the scope of this work to go into the
Biosorption can be used to eliminate heavy metals engineering details of the implementation of ow-
from industrial efuents or to recover precious metals through column systems. However, as outlined earlier,
from processing solutions. The fully loaded biosor- it is the natural ion-exchange property of the biomass
bent may concentrate heavy metals a thousand fold that lends itself to the task of selective removal of toxic
from their concentration in the liquid phase. This divalent heavy metals. This review is intended to
loading of the biomass may be reversed in order to highlight factors that need to be considered in investiga-
desorb the metals and several studies have shown tions of the relationship between substrate biochemistry
[41,67,68] elution of the biomass by acid aqueous and heavy metal binding mechanisms in the biosorption
solutions to be highly effective. The elution process process. In this regard, it is clear that the critical
does not signicantly reduce the binding capacity of the parameters in brown algal biosorption systems are the
biomass and several cycles may be employed. For alginate content and its specic macromolecular con-
example, Yang [86] used a Sargassum fluitans loaded formation in the brown algae. Our research group has
x-bed column to study uranium biosorption. He used a focused on developing Sargassum biomass biosorption
0.1 N HCl solution to elute the bound uranium and technology for both recovery of strategic metals as well
recovered 99.5% of the metal. Furthermore, the column as detoxication of heavy metal bearing industrial
was maintained continuously for 1 month over which wastes. Several investigations (e.g. [6972]) have speci-
time ve biosorptiondesorption cycles were carried out. cally focused on the implementation of ow-through
The biosorption capacity of the substrate decreased by column systems with mock-waste feed solutions in the
approximately 7% after the rst cycle and was about mM range (e.g. [69]). These studies, coupled with
20% less than the fresh biomass on the fth cycle. The equilibrium batch experiments, have consistently de-
observed drop in biosorption capacity between cycles monstrated that selectivity of Sargassum biomass is a
was attributed to leaching of alginate. The overall key feature in the design of such systems. The relative
metal concentration factor, dened as the ratio of the afnity of this raw biomass for various divalent metal
elution concentration to the inuent concentration for a cations was determined at environmentally relevant
given biosorption cycle, was determined to be approxi- concentrations to be
mately 25.
Cu > Ca > Cd > Zn > Fe
With a high concentration factor, it should be possible
to reduce the volume of waste that is produced by and is well reected by the breakthrough curves which
applying an iterative metal sorptiondesorption process evolve following passage of the simulated waste-feed
such that only a small volume of solid waste is streams through Sargassum packed columns. This is
ARTICLE IN PRESS
T.A. Davis et al. / Water Research 37 (2003) 43114330 4327
Fig. 11. Schematic diagram of possible biosorption implementation using packed bed columns for biosorption and desorption.
consistent with the divalent metalalginate gelation One of the outstanding tasks in evaluating the role of
sequence of Haug and Smidsr^d [35] discussed above. brown algal polysaccharides in metal binding is the
What is therefore important to recognize is that divalent determination of the extent to which the structure of the
metal ion sequestration by brown algae in the context of alginate and its hompolymeric guluronic acid content, or
remediation should be viewed as being a direct G-block structure determine selectivity among various
consequence of the formation of network junctions by metals. An identication of the biochemical factors that
the cations of homopolymeric guluronic acid blocks. control this parameter, coupled with a determination of
Although the ion-exchange properties of alginates and its alginate content, should allow us to predict the
raw algal biomass have been thoroughly documented in sorption behavior of brown algal biomass.
the elds of marine biochemistry, food technology and A complete characterization of brown algal substrate
metal bioremediation, the selective binding behavior biochemistry will be necessary to credibly emphasize the
observed in ow-through remediation systems can now advantages of biosorption over conventional ion-ex-
be specically attributed to the presence of abundant change resins and materials. The biochemical concepts
G-blocks. used in dening the equilibrium state and heavy metal
binding mechanisms are becoming more realistic than
ever. Nevertheless, whereas important advances in
6. Conclusions knowledge have been realized in recent years, the goals
stated earlier are paramount toward the implementation
The brown algae represent an especially efcient and of biosorption technology in industrial and environ-
resilient class of biosorbents relative to other biomass mental remediation.
types. Fortunately, due to their economic value in many
industrial applications, there is much information about
their basic structure and biochemical constitution. This Acknowledgements
in turn makes the interpretation of the sorption
behaviors and elucidation of metal binding mechanisms We wish to acknowledge our colleague, Dr. Silke
more rigorous. The order Laminariales and Fucales of Schiewer whose previous work greatly inuenced this
the brown algae (division Phaeophyta) are the most text. This work was made possible by a Natural Sciences
important groups of algae to the eld of biosorption and Engineering Research Council of Canada (NSERC)
because of the abundance of their cell wall matrix Seed Grant to A.M. Additional nancial support was
polysaccharides and extracellular polymers. The alginate provided by individual NSERC Research grants to
polysaccharide is mainly responsible for the natural ion- A.M. and B.V. as well as funding from NSERC and the
exchange capacity of the brown algae. Its unique Fonds pour la Formation des Chercheurs et lAide a" la
macromolecular structure gives rise to selective metal Recherche du Qu!ebec (FCAR) to T.D. in the form of a
binding whose mechanism is commonly represented by post-graduate scholarships. Finally, the authors would
the egg-box model. like to thank Prof. H. Seki and one anonymous journal
ARTICLE IN PRESS
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