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Algae of economic importance that accumulate cadmium and lead: A review

Abstract

Currently, algae and algae products are extensively applied in the pharmaceutical, cosmetic and food industries. Algae are the main organisms that take up and store heavy metals. Therefore, the use of compounds derived from algae by the pharmaceutical industry should be closely monitored for possible contamination. The pollution generated by heavy metals released by industrial and domestic sources causes serious changes in the aquatic ecosystem, resulting in a loss of biological diversity and a magnification and bioaccumulation of toxic agents in the food chain. Since algae are at the bottom of the aquatic food chain, they are the most important vector for transfer of pollution to upper levels of the trophic chain in aquatic environments. Moreover, microalgae are also used for the bioremediation of wastewater, a process that does not produce secondary pollution, that enables efficient recycling of nutrients and that generates biomass useful for the production of bioactive compounds and biofuel.

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825

ISSN 0102-695X

http://dx.doi.org/10.1590/S0102-

695X2012005000076

Received 29 Nov 2011

Accepted 29 Jan 2012

Available online 5 Jun 2012

Revista Brasileira de Farmacognosia

Brazilian Journal of Pharmacognosy

22(4): 825-837, Jul./Aug. 2012

Algae of economic importance that

accumulate cadmium and lead: A review

Priscila O. Souza,1 Lizângela R. Ferreira,2 Natanael R. X. Pires,2

Pedro J. S. Filho,3 Fabio A. Duarte,4 Claudio M. P. Pereira,¹

Márcia F. Mesko*,2

1Laboratório de Heterociclos Bioativos e Bioprospecção, Centro de Ciências Químicas,

Farmacêuticas e de Alimentos, Universidade Federal de Pelotas, Brazil.

2Laboratório de Controle de Contaminantes em Biomateriais, Centro de Ciências

Químicas, Farmacêuticas e de Alimentos, Universidade Federal de Pelotas, Brazil.

3Laboratório de Análise de Contaminantes Ambientais, Central Analítica, Instituto

Federal Sul-Riograndense, Brazil.

4Escola de Química e Alimentos, Universidade Federal do Rio Grande, Brazil.

Abstract: Currently, algae and algae products are extensively applied in the

pharmaceutical, cosmetic and food industries. Algae are the main organisms that take

up and store heavy metals. Therefore, the use of compounds derived from algae by the

pharmaceutical industry should be closely monitored for possible contamination. The

pollution generated by heavy metals released by industrial and domestic sources causes

serious changes in the aquatic ecosystem, resulting in a loss of biological diversity and

a magni cation and bioaccumulation of toxic agents in the food chain. Since algae are

at the bottom of the aquatic food chain, they are the most important vector for transfer

of pollution to upper levels of the trophic chain in aquatic environments. Moreover,

microalgae are also used for the bioremediation of wastewater, a process that does

not produce secondary pollution, that enables ef cient recycling of nutrients and that

generates biomass useful for the production of bioactive compounds and biofuel.

Keywords:

bioactive compounds

macroalgae

metals

microalgae

secondary metabolites

Introduction

Environmental contamination by heavy metals

is a growing global problem, which is directly related to

anthropogenic actions. For this motive, many techniques

for environmental remediation of heavy metals are being

studied (Ofer et al., 2003; Bayramoğlu et al., 2006; Rai,

2008, 2010; Rawat et al., 2011). Among these techniques,

the application of microorganisms has been widely

discussed, mainly in view of their capability to remove

pollutants from aquatic environments with good ef ciency

and relatively low cost. In this context, macroalgae and

microalgae have special properties that can be used

as a powerful technology to reduce environmental

contamination.

In particular, intense human activities can

result in high metal concentrations in the environment,

leading to numerous problems (Phillips, 1995;

MacFarlane & Burchett, 2001). Thus, although low

concentrations of some heavy metals are metabolically

important to many living organisms, at higher levels

they can potentially be toxic (Phillips, 1995; Sunda &

Huntsman, 1998; Pinto et al., 2003a). The pollution

generated by heavy metals released from industrial and

domestic sources causes serious changes in the aquatic

ecosystem, resulting in a loss of biological diversity

and the magnification and bioaccumulation of toxic

agents in the food chain (He et al., 1998).

Aquatic ecosystems such as rivers, ponds

and lakes are mainly affected by pollutants and heavy

metals discharged in industrial effluents and represent

a potential risk to the health of humans and ecosystems

(Rai, 2010). According to Rai (2008), several new

technologies have been developed for the removal

of heavy metals from wastewaters in a feasible way.

Nonetheless, these techniques are often only partially

effective and of relatively high cost, which can be

an obstacle to large-scale investment. Although trace

metals can be toxic to aquatic organisms and can be

accumulated by several marine species (Bargagli et al.,

1996), recent research has shown that some bacteria,

fungi, mussels, fishes and algae have the capability

to absorb trace metals and thus have the potential to

serve as economically viable biological materials for

the reduction of environmental pollution (Lourie et al.,

2010).

Some metals and their compounds have been

linked to mechanisms of carcinogenicity and metals

Article

Algae of economic importance that accumulate cadmium and lead: A review

Priscila O. Souza et al.

Rev. Bras. Farmacogn. Braz. J. Pharmacogn. 22(4): Jul./Aug. 2012

826

such as cadmium and lead have been widely studied

in view of their potential carcinogenicity to humans

(Beyersmann & Hartwig, 2008). In addition, oxidative

stress in living organisms can be related to the toxicity

of metals, involving an increase in the concentration

of reactive oxygen species and/or a reduction in the

cellular antioxidant capacity (Pinto et al., 2003a).

Oxidative stress can be associated with the inhibition of

photosynthesis, of chlorophyll production or of growth

in primary producers. These toxic effects can result

from exposure to high concentrations of metals or to

exposure of lower concentrations for longer periods,

reflecting the fact that the toxicity of heavy metals is

largely dose-dependent (Baumann et al., 2009). It has

been shown that the photosynthesis of some species

of macroalgae can be affected by the accumulation of

heavy metals (Gledhill et al., 1997; Baumann et al.,

2009). Collen et al. (2003) observed that copper (Cu) and

cadmium (Cd) induced oxidative stress in Gracilaria

tenuistipitata Zhang & Xia, a red macroalgae in the

Gracilariaceae (Rhodophyta) family. Moreover, due to

the release of heavy metals and other contaminants into

the environment, the difficulty of cultivating Gracilaria

has increased (Tonon et al., 2011). Some authors (Pinto

et al., 2003a; Torres et al., 2008) have pointed out that

exposure to these elements can be a barrier to the growth

of many marine organisms, including phytoplankton

and macroalgae, which could eventually result in a

decrease in biodiversity. Of particular importance is

the finding that the lipid composition of algae can be

altered by the influence of heavy metals (Vavilin et al.,

1998; Rocchetta, et al., 2006). At the same time, it is

well known that the oxidation of lipids can occur as a

result of oxidative stress, reflecting the production of

reactive oxygen/nitrogen species (Pinto et al., 2003b;

Leitão et al., 2003). In other experiments (Okamoto et

al., 2001; Collen et al., 2003; Rocchetta et al., 2006),

it was demonstrated that the levels of polyunsaturated

fatty acids (PUFA) are more affected, suffering a

greater decrease in the presence of heavy metals.

According to Pinto et al. (2011), Cd2+ was more toxic

than Cu2+ and greatly reduced the PUFA concentration

in G. tenuistipitata. Here it is important to note that

Gracilaria is an increasingly important source of

secondary metabolites with antimicrobial, antioxidant

and antitumoral activities, principally terpenes, several

fatty acids and nitrogenous compounds (Cardozo et al.,

2007; Boobathy et al., 2010; Zandi et al., 2010; Falcão

et al., 2010; Tonon et al., 2011).

The biosorption capacity of the green algae

species Spirogyra spp. and Cladophora spp. To

accumulate lead (Pb2+) and copper (Cu2+) from aqueous

solutions was evaluated by Lee & Chang (2011). On the

basis of continuous adsorption-desorption experiments,

these authors reported that both algal species were

excellent biosorbents, with potential for further

development. The microalgae Spirogya spp. adsorbed

between 10-40 mg g-1 of Pb2+ and between 45-90 mg

g-1 of Cu 2+ from aqueous solutions containing different

concentrations of Pb2+ and Cu2+. By comparison, the

algae Cladophora spp. adsorbed between 5-10 mg g-1

of Pb2+ and between 30-45 mg g-1 of Cu2+ .

Several studies have explored the metal binding

properties of different biosorbents such as fungi, yeasts,

bacteria and algae (Volesky & Holan, 1995; Kapoor &

Viraraghavan, 1995). Numerous studies have employed

macroalgae and microalgae for the biosorption of

metals and the ability of certain species of macroalgae

to accumulate and tolerate high levels of metals has

been demonstrated. Hence, algae represent an effective,

economically viable and environmentally friendly (Yu

et al., 1999) alternative for the bioremediation of heavy

metals, especially cadmium and lead, the two metals that

are subject of the present review.

Bioremediation

Heavy metals discharged into the environment

tend to persist indefinitely, sometimes accumulating in

living organism via food chain, and are thus considered

to represent a potentially serious environmental threat

(Kuppusamy et al., 2004). The most effective and

least expensive methods for the remediation of waters

contaminated by heavy metals have been the focus of

much research in recent decades, with the objective of

reducing the risk to public health caused by the presence

of these wastewater contaminants (Kumar et al.,

2009). Compared to conventional treatment methods,

biosorption stands out because of the following

advantages: high efficiency of removal of metals from

dilute solutions; low cost; and minimization of chemical

and/or biological sewage. Moreover, it does not require

addition of nutrients or regeneration of the biosorbent

and makes it possible to recover the metals (Kratochvil

& Volesky, 1998). According to Goyal et al. (2003),

the biosorption of metals can be performed by many

different microorganisms, including bacteria, yeast,

fungi and algae. Schiewer & Patil (1997) reported that

the efficiency of different biosorbents for the removal

of heavy metals can depend on the pH of the solution.

Due to stricter government regulations, there

has been a growing interest in cost-effective remediation

technologies (Davis et al., 2003). In this context,

bioremediation of polluted areas and wastewater can be

an economically viable alternative, especially when the

sorbent can be recycled and the heavy metals recovered

for resale. Remediation of heavy metals encourages

environmental awareness and ameliorates the effects

of pollution (Salt et al., 1995). Bioremediation uses

naturally occurring biomass as the substrate for

Algae of economic importance that accumulate cadmium and lead: A review

Priscila O. Souza et al.

Rev. Bras. Farmacogn. Braz. J. Pharmacogn. 22(4): Jul./Aug. 2012 827

chelation of the metal ions, either passively or through

non-metabolically mediated processes (Baumann et al.,

2009).

Given their abundance in various environmental

systems, their adaptability to different environmental

conditions (Rajfur et al., 2010) and their ability to

accumulate large amounts of heavy metals such as

cadmium, lead, zinc, copper, chromium, and manganese

(Anastasakis et al., 2011), algae appear to be the most

appropriate microorganism for monitoring pollution of

water resources by heavy metals (Wallenstein et al., 2009;

Rajamani et al., 2007). Indeed, algae have been used for

over 40 years for the treatment of wastewater, the rst

application being described by Oswald & Gotaas (1957).

More recently, John (2000; Rawat et al., 2011) introduced

the term phycoremediation to refer to remediation by

algae. In this context, it is important to emphasize that

phycoremediation has several applications in addition to

the removal of metals. These include the: (i) removal of

nutrients from municipal wastewater and from efuents rich

in organic matter; (ii) removal of nutrients and xenobiotic

compounds with the help of biosorbents based on algae;

(iii) treatment of acidic wastewater and metals; (iv)

sequestration of CO2; (v) transformation and degradation

of xenobiotics; and (vi) detection of toxic compounds with

algae-based biosensors (Rawat et al., 2011).

Many intrinsic and extrinsic factors can

influence the accumulation of metals by algae, such

as cellular activity, exposure time, chelating species,

and environmental factors such as pH, salinity, organic

matter, and temperature (Runcie & Riddle, 2004).

Furthermore, structural differences between species

influence their absorption capacity (Favero & Frigo,

2002). For the macroalgae Durvillaea antarctica

(Chamisso) Hariot, Runcie & Riddle (2004) observed

a low metal content that could be ascribed to the low

availability of the metals in the surrounding waters.

Recently, macroalgae have been increasingly

used as a tool for monitoring marine environments

contaminated by heavy metals (Daka et al., 2003;

Stengel et al., 2004; Daby, 2006, Baumann et al.,

2009; Kumar et al., 2009; Tonon et al., 2011). Many

macroalgae are able to accumulate high levels of trace

metals, which are sometimes larger than those found

in water samples from the same site (Cardwell et al.,

2002; Salgado et al., 2006).

In order to determine the heavy metals present

in environmental samples, analytical techniques such

as atomic absorption spectrometry (AAS) (Carrilho

et al., 2003; Zhang & O'Connor, 2005) have been

widely used due to the relatively low cost. However,

inductively coupled plasma mass spectrometry (ICP-

MS) and inductively coupled plasma optical emission

spectrometry (ICP OES) have been increasingly used

for metal determination in view of their much lower

limits of detection and the capability of multielement

detection when coupled with suitable sample preparation

procedures (Mesko et al., 2011; Soares et al., 2012).

In the remainder of this review, we shall

concentrate on two especially toxic heavy metals,

cadmium and lead, and their biosorption by micro- and

macroalgae.

Cadmium

Cadmium stands out among the heavy metals

because it is relatively easily removed from waste

streams, primarily due to its ability to form stable

complexes with several different ligands (Ofer et al.,

2003). The presence of cadmium in natural waters is

extremely undesirable since it is both toxic and a non-

essential element for most living organisms (Leborans

& Novillo, 1996; Farias et al., 2002).

In a recent research, Tonon et al. (2011)

evaluated the absorption of cadmium (Cd) and copper

(Cu) by three species of Gracilaria: G. tenuistipata

Zhang & Xia cultivated in the laboratory and exposed

to the metal and G. birdiae Plastino & Oliveira and

G. domingensis (Kützing) collected in their natural

environments. G. tenuistipitata bioaccumulated higher

concentrations of Cu than Cd, showing that this

macroalgae is a metal bio-accumulating organism; the

biological function of the accumulated Cd, if any, is

currently unknown.

Stohs & Bagchi (1995) suggested that Cd

ions might displace zinc and iron from proteins. This

could potentially have deleterious consequences for

seaweed growth because the liberation of iron ions

might induce the Fenton reaction, producing reactive

oxygen species (ROS) and total oxidative stress. In

land plants, Cd competes for divalent ion carriers and

can be transported with protons and type P ATPases.

According to Guerinot (2000), the ability to compete

for essential metal carriers is particularly important for

cadmium (Cd), mercury (Hg) and lead (Pb). Baumann

et al. (2009) evaluated the Cd concentration in seven

algal species and noted that 10 mmol L-1 cadmium ion

led to the greatest increase in Cd accumulation. The

macroalgae Palmaria palmata (Linnaeus) Kuntze had

the highest concentrations of Cd and Ascophyllum

nodosum (Linnaeus) the lowest. Despite the fact that

P. palmata accumulated the highest amounts of Cd

and showed a significant reduction in fluorescence, no

correlation was found between Cd accumulation and

its toxicity. Küpper et al. (1996, 1998) demonstrated

that photosynthesis can be affected by exposure to Cd

and Zn, which can replace the Mg2+ in the chlorophyll

molecule, affecting its light-harvesting ability.

Algae of economic importance that accumulate cadmium and lead: A review

Priscila O. Souza et al.

Rev. Bras. Farmacogn. Braz. J. Pharmacogn. 22(4): Jul./Aug. 2012

828

Lead

Lead is a more pernicious contaminant in

aquatic environments and is rapidly accumulated by

organisms (Ribeiro et al., 2010). Moreover, it is able

to bind strongly to amino acids, enzymes, DNA and

RNA and can induce the production of reactive oxygen

species (ROS) like the superoxide radical and hydrogen

peroxide that can cause severe oxidative damage

to plant cells (e.g., by increasing membrane lipid

peroxidation and permeability) (Apel & Hirt, 2004).

Lead can inhibit the synthesis of chlorophyll because

it changes the absorption of essential elements such as

Mg and Fe (Sunda & Huntsman, 1998).

The biological functions of lead in algae

are unknown (Pawlik-Skowronska, 2000), but lead

is known to have adverse effects on microalgal

morphology, growth and photosynthesis when present

at high concentrations (Pawlik-Skowronska, 2002).

Baumann et al. (2009) showed that for brown

algae there was signicant variation in Pb concentrations

for all seven species of algae examined. Lead proved to

be less toxic than the other ve metals evaluated, but was

accumulated to a greater extent by all seven algae tested

than the other metals. Moreover, none of the treatments

with lead affected the uorescence yield of either species.

According to Miles et al. (1972), lead affects light

absorption by PSI and PSII and the chloroplast coupling

factor. However, Baumann et al. (2009) demonstrated

that lead was the only metal out of ve tested that did not

reduce chlorophyll uorescence in the species evaluated.

The results indicaated that macroalgae, especially Ulva

intestinalis Linnaeus, are promising organisms for the

bioremediation of waters contaminated by lead, because

of their apparent tolerance to Pb and their ability to

accumulate lead at high rates.

Applications of algae in the pharmaceutical industry

and in environmental remediation

The pharmaceutical industry has shown great

interest in the use of algae as a source of biochemically

active substances (Burja et al., 2001, Singh et al., 2005,

Blunt et al., 2005, Guaratini et al, 2005; Cardozo et

al., 2008; Cardozo et al., 2009; Guaratini et al., 2009).

The fact that algae may produce chemical prototypes of

new therapeutic agents has stimulated bioprospecting

for new algal secondary metabolites and the

synthetic modification of compounds with potential

pharmaceutical applications (Cardozo et al., 2007). In

addition to novel biologically active substances, algae

also provide compounds essential to human nutrition

(Burja et al., 2001; Gressler et al., 2010).

Cardozo et al. (2006; 2007) described the main

substances biosynthesized by algae with a potential

economic impact on nutrition, public health and the

pharmaceutical industry. The diversity of compounds

synthesized by marine algae via a variety of metabolic

pathways is the result of the defense strategies that

they have developed in order to survive in a highly

competitive environment. Hence, many of these

secondary metabolites are chemically distinct from

those found in terrestrial organisms (Burja et al., 2001;

Singh et al., 2005; Blunt et al., 2005; Carignan et al.,

2009; Wijesinghe & Jeon, 2011). According to Kamatou

et al. (2008), the presence of these compounds may

help explain some of the traditional uses of medicinal

plants.

Algae are ecologically important because

they occupy the base of the food chain in aquatic

ecosystems and produce half of the O2 and the majority

of the dimethylsulfide released into the atmosphere. In

addition, algae are the main source of food for bivalve

mollusks in all stages of growth, for zooplankton

(rotifers, copepods and brine shrimp) and for the larval

stages of crustaceans and some species of fish (Cardozo

et al., 2007) .

The quality of the food transferred to the

higher trophic levels of the food chain is determined by

the chemical composition of algae (such as fatty acids,

sterols, amino acids, sugars, minerals and vitamins)

(Brown & Miller, 1992; Di Mascio et al., 1995;

Guaratini et al., 2007; Dhargalkar & Verlecar, 2009).

The nutritional value of algal species depends on

several characteristics such as size, shape, digestibility

and toxicity (Cardozo et al., 2007). The Chinese,

Japanese and Korean diet includes the consumption of

several species of red and brown algae (Dawczynski et

al., 2007). In addition to this traditional use in the East,

people in many other parts of the world also consume

or come into contact with algae-derived products

used as additives in manufactured food products and

processed meat and fruit or in everyday materials such

as toothpaste, paint, solid air fresheners and cosmetics

(Gressler et al., 2009; 2011).

Algal biomass can be effectively applied in

bioremediation because the proteins and polysaccharides

of their cell walls can contain anionic carboxylate,

sulfate or phosphate groups, which are optimal binding

sites for metals (Farias et al., 2002). Several studies have

shown that it is possible to enhance the accumulation of

metals by algal biomass. Thus, Kumar & Gaur (2011)

observed that pretreatment with CaCl2 generated new

sites for metal ion binding by inducing cross-linking

between the polymer chains of the exopolysaccharides

present in the biomass. Mehta et al. (2002) and Kalyani

et al. (2004) found that pre-treatment with HCl increased

the metal binding capacity of biomass (by 39 or 70%,

respectively), presumably be removing cationic species

that were bound to the anionic functional groups,

Algae of economic importance that accumulate cadmium and lead: A review

Priscila O. Souza et al.

Rev. Bras. Farmacogn. Braz. J. Pharmacogn. 22(4): Jul./Aug. 2012 829

making them available for binding of additional metal

ions. An improvement in the biosorption capacity for

metal ions could also be induced by an alkaline pre-

treatment, reflecting increased deprotonation of the

acidic functional groups of the biomass (Sampedro et

al.. 1995; Mehta & Gaur, 2001; Nagase et al., 2005;

Singh et al., 2007, 2008).

The performance of treatment systems using

algal biomass can be reduced by the presence of

chelating agents, such as fulvic acid, that can compete

with the anionic groups of algal biomass for binding of

metal ions (Pascucci & Kowalak, 1999). In addition,

there is a decrease in the percentage of metal removed

at higher metal concentrations (Pujari & Chandra,

2000) due to the saturation of the available metal

binding sites (Dönmez & Aksu, 2002). In this case, the

use of a greater amount of biomass may not enhance the

overall extent of metal ion binding if the metal ions that

initially bind to a dense layer of cells create a screening

effect (Zulkali et al., 2006).

Macroalgae

Seaweeds represent a significant portion of

global biodiversity. They constitute a large and diverse

group of organisms that play vital ecological roles in

marine communities and can be classified into three

categories according to their pigmentation: brown, red

and green algae (Wijesinghe & Jeon, 2011).

Seaweeds are a potentially renewable marine

resource and are known to be extremely rich in

bioactive compounds (Chandini et al., 2008; Kladi et

al. 2004) with novel biological activities (Kashman &

Rudi, 2004; Plaza et al., 2008). The brown seaweeds

or Phaeophyceae are noted for producing a range

of active components, including unique secondary

metabolites such as phlorotannins (Wijesinghe & Jeon,

2011). In addition, several components of brown algae

have been explored for their antioxidant, antiallergic,

antiinflammatory, antiwrinkling and whitening

properties.

Compared to other types of biomass, brown

algae showed the highest metal binding capacity, making

them particularly attractive for the bioremediation of

toxic heavy metals (Ofer et al., 2003). According to

Davis et al. (2003), the linear polysaccharides known

as alginate, which are present in gel form in the stem

of algae, are responsible for the biosorption of heavy

metals by these algae. Moreover, they noted that the

orders Laminariales and Fucales are probably the largest

seaweeds, and are the most abundant and widespread,

enhancing their potential for cost-effective application

in bioremediation. Macroalgae are usually sessile and

accumulate metals over time, so that differences in the

metal content of macroalgae depend on whether they

are located near and far from sources of pollution and

can be used to infer the source of metal contamination

(Runcie & Riddle, 2004). However, as pointed out

by Singh et al. (2007), this application does have its

limitations because of the confinement of seaweeds

to coastal areas and the difficulty of collecting them

during the metal sorption process.

In a comparative study reported by Kumar et

al. (2009), the ability to accumulate cadmium and lead

was evaluated for five green marine macroalgae by

employing initial metal concentrations in the range of

20 to 80 mg L-1 and different contact periods. The Pb

uptake values for Cladophora fasicularis (Mertens ex

C. Agardh) Kützing ranged from 5.68 to 33.53 mg g-1 ,

while Cd uptake values ranged from 4.08 to 18.78 mg

g-1 . The Cd uptake values for Ulva lactuca varied from

3.89 to 7.84 mg g-1 and those for Pb uptake from 6.19

to 25.07 mg g-1. For Chaetomorpha sp, the Pb uptakes

were between 7.52 and 35.08 mg g-1 and the Cd uptakes

between 7.98 and 31.55 mg g-1. Caulerpa sertularioides

(S.G.Gmelin) M.A.Howe showed Cd uptake values in

the range of 1.19 to 20.51 mg g-1 and Pb values in the

range of 6.03 to 21.58 mg g-1. Valoniopsis pachynema

(G. Martens) Borgesen had Cd uptakes in the range of

7.69 to 17.31 mg g-1 and Pb uptakes from 6.42 to 37.71

mg g-1. The efficiency of cadmiun absorption varied

in the order: Chaetomorpha sp. > C. sertularioides

> C. fasicularis > V. pachynema > U. lactuca ; for

lead, the corresponding order was: V. pachynema >

Chaetomorpha sp. > C. fasicularis > U. lactuca > C.

sertularioides. During the experimental exposure of the

seaweeds to these two heavy metals, the concentration

of free metal ion decreased significantly, demonstrating

that seaweeds can be excellent biosorbents.

Figueira et al. (2000) used several species of

the brown seaweeds Durvillaea sp., Laminaria sp.,

Ecklonia sp. and Homosira sp., pre-saturated with Ca,

Mg and K, and Hashim & Chu (2004) examined seven

species of brown, green and red seaweeds in order to

assess their ability to remove cadmium from aqueous

medium.

Gosavi et al. (2004) demonstrated that four

genera of macroalgae (Ulva sp., Enteromorpha sp.,

Chaetomorpha sp. and Cladophora sp.) accumulated

significant amounts of Fe, Al, Zn, Cd, Cu, As and Pb,

noting that cadmium was absorbed better by Cladophora

sp. (1.6±0.3 mg g-1 ), while Chaetomorpha sp. and

Enteromorpha sp. absorbed lead better. According to

Thomas et al. (2003), brown algae are the most effective

and promising substrates for Pb accumulation. Farias

et al. (2002) evaluated eleven species of macroalgae

from the Antarctica; the highest levels of trace metals

were found in Monostroma hariotii Gain and Phaeurus

antarcticus Skottsberg. However, M. hariotii was not

able to accumulate As, Cd and Pb, which are relevant

Algae of economic importance that accumulate cadmium and lead: A review

Priscila O. Souza et al.

Rev. Bras. Farmacogn. Braz. J. Pharmacogn. 22(4): Jul./Aug. 2012

830

because of their potential toxicity to living organisms.

Table 1 provides an annotated compendium of literature

reports published in the last decade on the application

of macroalgae for the biosorption of metals.

Microalgae

As an important biological resource with

multiple applications, microalgae have attracted great

interest (Sigaud-Kutner et al., 2002; Pinto et al.,

2003b; Rawat et al., 2011). At the same time that they

bioremediate wastewater, they provide biomass that

can be used to sequester carbon dioxide (Olguin, 2003;

Munoz & Guieyesse, 2006; Briens et al., 2008; Singh &

Gu, 2010 ) and to produce biofuels (methane, ethanol,

hydrogen, butanol etc.). Particularly advantageous

features of microalgae as a source of biomass for the

production of biodiesel include a high growth rate and

short regeneration time, a high lipid content, the minimal

requirement of land area, and the use of wastewater as

the source of nutrients for growth, without the use of

chemicals such as herbicides and pesticides (Rawat

et al., 2011). The main disadvantage is the difficulty

of separation of the microalgae, which are usually

unicellular, from their suspensions (Moreno-Garrido,

2008).

The growth of microalgae can be indicative of

water pollution since they typically respond to ions and

toxins (Rawat et al., 2011). Thus, the remediation of

wastewater by using microalgae is an environmentally

friendly process that does not generate secondary

pollutants and yields biomass that can be reused,

enabling efficient recycling of nutrients (Munoz &

Guieyesse, 2006). Besides their use in bioremediation

and biofuel production, microalgae can also be used

as additives in animal feed and for the extraction of

added-value products such as carotenoids and other

biomolecules (Rawat et al., 2011; Hobuss et al., 2011;

Soares et al., 2012).

The release of municipal and industrial

wastewater into bodies of water results in serious

environmental changes (Arora & Saxena, 2005; Bashan

& Bashan, 2010). Eutrophication, induced by a richness

of organic matter and of inorganic chemicals such as

phosphates and nitrate, can be particularly problematic

(Olguin, 2003; Godos et al., 2009; Bashan & Bashan,

2010). Eutrophication can be avoided with microalgae

because they use the wastewater as a food source for

their growth (Rawat et al., 2011) and the accumulation

of biomass (Munoz & Guieysse, 2006; Pittman et al.,

2011). A wide range of microalgae, such as Chlorella

sp., Scenedesmus sp., Phormidium sp., Botryococcus

sp., Clamydomonas sp. and Spirulina sp. (Olguin, 2003;

Chinnasamy et al., 2010; Kong et al., 2010; Wang et al.,

2010), can be effectively employed to treat domestic

wastewater. Using a consortium of 15 isolated native

algae, Chinnasamy et al. (2010) found > 96% removal

of nutrients from treated wastewater.

The rapid decline in the levels of metals,

nitrates and phosphates in wastewater upon microalgal

treatment (Wang et al., 2010), demonstrates the

efficiency of microalgae for the removal of metals and

nutrients, while meeting the stringent requirements of

international standards (Rawat et al., 2011).

Microalgae are a source of peptides with the

special ability to bind heavy metals (Perales-Vela,

2006). These proteins form organometallic complexes

that partition into the vacuoles to facilitate control of

the cytoplasmic concentrations of metal ions, thereby

preventing or neutralizing their potential toxic effects

(Cobbett & Goldsbrough, 2002). Prokaryotes use a

mechanism that is different from that of eukaryotes,

which use the consumption of ATP to drive the efflux of

heavy metals or enzymatic changes in metal speciation

for detoxification (Nies, 1999). These peptides can be

classified into two categories: (Robinson, 1989; Rauser,

1990; Steffens, 1990; Thiele, 1992):

1. Short-chain polypeptides, synthesized

enzymatically and called phytochelatins or class III

metallothioneins, are found in higher plants, algae and

certain fungi;

2. Proteins encoded by genes, which include the

class II metallothioneins (found in cyanobacteria, algae

and higher plants) and class I metallothioneins (found in

most vertebrates, in Neurospora and Agaricus bisporus,

but with no records so far in algae).

Initially, when the short-chain polysaccharides

were discovered they were named phytochelatins (PC)

because they were isolated from higher plants, explaining

the prex 'phyto", and had the ability to chelate cadmium

ions (Grill et al., 1985; Steffens, 1990). However, the

class II metallothioneins proved to be effective in plant

responses to stress by heavy metals and the name of the

PC was changed to class III metallothioneins (Mt III)

(Rauser, 1990). Howe & Merchant (1992) showed that the

microalgae Chlamydomonas reinhardtii P.A. Dangeard

could sequester about 70% of the cadmium present in the

cytosol by the action of Mt III.

In a study by Avilés et al. (2003) with the

agellated protist Euglena gracilis exposed to cadmium,

79% of the metal was accumulated in mitochondria and

there was an increase in the concentration of Cys and

glutathione in cells treated with cadmium. In addition,

17% of the total Mt III found in the treated cells was

concentrated in the mitochondria. According to Mendoza-

Cózatl et al. (2004), the presence of Mt III and Cd2+ in

chloroplasts and mitochondria of Euglena may be the

result of the following processes:

(1) the Mt III are synthesized and sequester

Cd2+ in the cytosol; the Cd-Mt III complexes are then

Algae of economic importance that accumulate cadmium and lead: A review

Priscila O. Souza et al.

Rev. Bras. Farmacogn. Braz. J. Pharmacogn. 22(4): Jul./Aug. 2012 831

subsequently transported inside the chloroplast and

mitochondria;

(2) the Mt III are synthesized in these two

organelles and bind Cd2+ transported as free ions,

forming the HMW complexes;

(3) both processes co-exist and the Mt III are

synthesized in the three cellular compartments.

Microalgae are often grown in two commercial

systems: open raceway ponds and closed photobioreactors

(Hollnagel et a;, 1996; Chisti, 2007; Munoz & Guieyesse,

2006; Chinnasamy et al., 2010). The former system is

inexpensive and allows the removal of nutrients from

domestic wastewater, while photobioreactors, despite

increased productivity, and not feasible on a large scale

for phycoremediation due to economic limitations

(Chinnasamy et al., 2010). The separation of algal

biomass can be accomplished by methods such as

centrifugation, occulation, sedimentation, microltration

and combinations of these (Grima et al., 2003; Munoz &

Guieyesse, 2006; Danquah et al., 2009; Mutanda et al.,

2011). Hobuss et al. (2011) reported a preliminary study of

biodiesel production by the microalgae Chlorella vulgaris

Beijerinck cultivated in a photobioreactor; the biodiesel

was obtained in a signicantly shorter time and with good

lipid productivity.

The use of high rate algal ponds (HRAP) for

the treatment of wastewater results in the production of

large amounts of algal biomass, which can be converted

into biofuels in many ways, including anaerobic

digestion to give biogas, transesterification of lipids

to obtain biodiesel, fermentation of carbohydrates into

bioethanol and high temperature conversion to bio-crude

oil (Mesple et al., 1996; Munoz & Guieyesse, 2006;

Park et al., 2011). Moreover, HRAP are an effective

system for phytoremediation, replacing conventional

tertiary treatment nutrient removal, which has a cost

four times higher than that of conventional primary

treatment (Mesple et al., 1996; Olguin et al., 2004;

Moreno-Garrido, 2008; Godos et al., 2009; Garcia et al.,

2009). The main advantages of this treatment are that

microalgal photosynthesis releases oxygen and there is

no need for mechanical aeration because the microbial

degradation of organic matter is heterotrophic.

Considering the ability of microalgae to

degrade organic pollutants, dangerous species of

Chlorella sp., Ankistrodesmus sp. and Scenedesmus sp.

have demonstrated success in the treatment of refinery

wastewater and wastewater from paper mills (Pinto et

al., 2002). Cerniglia et al. (1979, 1980) evaluated the

ability of algae to biodegrade the organic pollutants

present in municipal waste by stimulating cell growth in

the presence of pollutants; they found that cyanobacteria

and eukaryotic microalgae biotransformed naphthalene

into four main non-toxic metabolites (1-naphthol,

4-hydroxy-4-tetralone, cis-dihydronaphthalene diol

and trans-dihydronaphthalene diol).

Inthorn et al. (2002) showed that green microalgae

(C. vulgaris, Scenedesmus sp. Chlorococcum sp. and

Table 1. Applications of seaweeds for the biosorption of metals.

Seaweeds Elements Remarks References

Gracilaria tenuistipata Zhang & Xia, G.birdiae

Plastino & Oliveira, G.domingensis (Kützing)

Cd and Cu G. tenuistipitata was able to bioaccumulate higher

concentrations of Cu (0.13±0.03 µg g-1 ) than Cd

(<0.01 µg g-1)

Tonon et al.,

2011

Ascophyllum nodosum (Linnaeus) Le Jolis, Fucus

vesiculosus Linnaeus, Ulva intestinalis Linnaeus,

Cladophora rupestris (Linnaeus) Kützing, Chondrus

crispus Stackhouse, Palmaria palmata (Linnaeus)

Kuntze, Polysiphonia lanosa (Linnaeus) Tandy

Cd and Pb P. palmata had the highest concentrations of Cd

and A. nodosum the lowest. No correlation was

found between Cd accumulation and its toxicity. U.

intestinalis had apparent tolerance to Pb, as well as

the ability to accumulate it at high rates.

Baumann et al.,

2009

Chaetomorpha sp., Caulerpa sertularioides

(S.G.Gmelin) M.A.Howe, Cladophora fasicularis

(Mertens ex C. Agardh) Kützing, Valoniopsis

pachynema (G. Martens) Borgesen, Ulva lactuca

Cd and Pb Chaetomorpha sp. accumulated more Cd than U.

lactuca; and V. pachynema amassed more Pb than

C. sertularioides.

Kumar et al.,

2009

Ulva sp., Enteromorpha sp., Chaetomorpha sp.,

Cladophora sp.

Fe, Al, Zn, Cd,

Cu, As and Pb

Cd was more absorbed by Cladophora sp.

(1.6±0.3 mg g-1 ), while the Chaetomorpha sp. and

Enteromorpha sp. absorbed more Pb

Gosavi et al.

(2004)

Ascoseira mirabilis Skottsberg, Palmaria decipiens

(Reinsch) R.W.Ricker, Desmarestia anceps Montagne,

Monostroma hariotti Gain, Adenocystis utricularis

(Bory de Saint-Vincent) Skottsberg, Desmarestia

antarctica R.L.Moe & P.C. Silva, Himantothallus

grandifolius (A.Gepp & E.S.Gepp) Zinova, Iridaea

cordata (Turner) Bory de Saint-Vicent, Phaeurus

antarcticus Skottsberg, Georgiella conuens (Reinsch)

Kylin, Myriogramme mangini (Gain) Skottsberg

As, Cd, Co, Cr,

Cu, Fe, Mn,

Mo, Ni, Pb, Se,

Sr, V, and Zn

Highest levels of trace metals were found in M.

hariotii and P. antarcticus; however, M. hariotii

was not able to accumulate As, Cd and Pb, which

are relevant given their toxicity potential for living

organisms.

Farias et al.,

2002

Algae of economic importance that accumulate cadmium and lead: A review

Priscila O. Souza et al.

Rev. Bras. Farmacogn. Braz. J. Pharmacogn. 22(4): Jul./Aug. 2012

832

Fischerella sp.) and cyanobacteria (Lyngbya spiralis

Geitler, Tolypothrix tenuis Kützing, Stigonema sp. and

Phormidium molle (Kützing) Gomont) efciently removed

Pb (II), Cd (II) and Hg (II) ions. Recently, there has been

a growing use of the unicellular microalgae C. reinhardtii

in bioremediation (Mace & Welbourn, 2000; Adhiya et

al., 2002). Bayramoğlu et al. (2006) isolated wild-type

C. reinhardtii from a polluted part of the Kizilirmak

river, taking advantage of the fact that species growing

in polluted areas have a higher resistance and ability to

accumulate heavy metals. They showed that Ca-alginate

bead with immobilized biomass of the microalgae were

biosorbents capable of removing Hg (II), Cd (II) and Pb

(II) ions from aqueous media.

The cyanobacterium Microcystis novacekii

(Komarek) Compère, present in many tropical countries,

is found in eutrophic and polluted environments (Singh,

1998), indicating that this species may be resistant to

exposure to toxic agents, including heavy metals (Pradhan

et al., 2007). According to Ribeiro et al. (2010), the

biomass of M. novacekii had a maximum sorption capacity

of 70 mg g-1 at 21±2 °C and pH 5.0, higher than that of

other biosorbents used to remove lead from water. The

use of active biomass was not feasible for the removal of

lead due to precipitation of the metal and cell growth was

inhibited by concentrations of free metal ions in excess

of 0.5 mg L-1. In contrast, inactive cells showed a high

capacity for absorbtion of Pb2+ from aqueous solution

and equilibrium was reached quickly. Some of the most

important applications of microalgae for the biosorption of

metals are outlined in Table 2.

Conclusion

Based on data obtained in a number of studies,

there is clear potential for the use of macroalgae and

microalgae for the bioremediation of metals. In addition,

there is somewhat of an advantage of microalgae over

macroalgae due to the ease of collection, preparation

and testing of the former. However, further studies of

metal biosorption by algae are needed in order to obtain

specific relationships correlating the affinities of algae

for certain metals with ecological, physiological,

biochemical and molecular parameters.

Acknowledgements

The authors thank the CNPq, CAPES,

FAPERGS and FAPESP for funding and fellowship

support.

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*Correspondence

Márcia F. Mesko

Laboratório de Controle de Contaminantes em Biomateriais,

Centro de Ciências Químicas, Farmacêuticas e de Alimentos,

Universidade Federal de Pelotas

Campus Capão do Leão, Caixa Postal 354, 96010-900

Pelotas-RS, Brazil

marcia.mesko@pq.cnpq.br

Tel: +55 53 3275 7387

Fax: +55 53 3275 7354

... Extreme changes in the aquatic environment are exacerbated by the pollution produced by heavy metals released by industrial and domestic sources, resulting in the depletion of ecological diversity and the magnification and bioaccumulation of food chain toxic agents. One of the environmental pollutants of significance is metals (Souza et al. 2012). ...

• Ashgan A. AbouGabal
• Asmaa Khaled
• · Haiam
• Shalaby

Understanding the diversity patterns of macroalgae assemblages in the coastal Mediterranean of Alexandria is important for seawater management. To elucidate the diversity patterns in macroalgae communities, five Mediterranean sites (Eastern Harbor (EH), Abu Talat (AT), El Mex Bay (EM), SidiBishir (SB) and El-Tabia pumping (TPS) were examined during June 2019. Macroalgae found on the Alexandria coast was 5 species namely, Ulva Fasciata, Ulva Compressa, Corallina Offici-nalis, Carollina Elongate and PetrocladiaCapillacea. Patterns of alpha and beta diversity were evaluated across macroalgal habitats, in relation to different levels of heavy metal accumulation and physicochemical parameters. We found significant spatial differences in alpha diversity and moderate value of the beta index (average ~ 0.6) explained by the high variation of pollution by heavy metals. The abundance of the Ulva fasciata is higher than those of other macroalgae. EH is the location that has the highest diversity index value (H'), the richness index of species (D), the highest evenness index (E), and Simpson index 1.28, 0.33, 0.59, and 0.69 respectively.

... Extreme changes in the aquatic environment are exacerbated by the pollution produced by heavy metals released by industrial and domestic sources, resulting in the depletion of ecological diversity and the magnification and bioaccumulation of food chain toxic agents. One of the environmental pollutants of significance is metals (Souza et al. 2012). ...

Understanding the diversity patterns of macroalgae assemblages in the coastal Mediterranean of Alexandria is important for seawater management. To elucidate the diversity patterns in macroalgae communities, five Mediterranean sites (Eastern Harbor (EH), Abu Talat (AT), El Mex Bay (EM), SidiBishir (SB) and El-Tabia pumping (TPS) were examined during June 2019. Macroalgae found on the Alexandria coast was 5 species namely, Ulva Fasciata, Ulva Compressa, Corallina Officinalis, Carollina Elongate and PetrocladiaCapillacea. Patterns of alpha and beta diversity were evaluated across macroalgal habitats, in relation to different levels of heavy metal accumulation and physicochemical parameters. We found significant spatial differences in alpha diversity and moderate value of the beta index (average ~ 0.6) explained by the high variation of pollution by heavy metals. The abundance of the Ulva fasciata is higher than those of other macroalgae. EH is the location that has the highest diversity index value (H'), the richness index of species (D), the highest evenness index (E), and Simpson index 1.28, 0.33, 0.59, and 0.69 respectively.

... Cd accumulation in S. fusiforme seedlings significantly affected the activities of antioxidants and antioxidizes. Under Cd stress, algae produce ROS to destruct the biological macromolecules, leading to reduced or inactive enzymes, and inducing the synthesis or activation of ROS-related clearance enzymes (Zhao et al., 2008;Souza et al., 2012), although it may also induce redox signals to regulate physiological processes (Kacperska, 2004). The large number of free radicals produced by high Cd stress promotes lipid peroxidation and causes severe damage to the biomembranes in plant cells, including cell membranes, and chloroplasts (Panda and Choudhury, 2005). ...

• Tiantian Zhang
• Minheng Hong
• Mingjiang Wu
• Zengling Ma

Cadmium (Cd) is a common heavy metal pollutant in the aquatic environment, generally toxic to plant growth and leading to growth inhibition and biomass reduction. To study the oxidation resistance in Sargassum fusiforme seedlings in response to inorganic Cd stress, we cultured the seedlings under two different Cd levels: natural seawater and high Cd stress. High Cd stress significantly inhibited the seedlings growth, and darkened the thalli color. Additionally, the pigment contents, growth rate, peroxidase (POD) activity, dehydroascorbic acid (DHA) content, and glutathione reductase (GR) activity in S. fusiforme were significantly reduced by high Cd treatment. Contrarily, the Cd accumulation, Cd2+ absorption rate, dark respiration/net photosynthetic rate (Rd/Pn), ascorbic acid (Vc) content, soluble protein (SP) content, glutathione (GSH), and the activities of superoxide dismutase (SOD) and catalase (CAT) of S. fusiforme under Cd treatment significantly increased compared to the control group. The decrease of malondialdehyde (MDA) was not significant. Although S. fusiforme seedlings increased the antioxidant activities of POD, SOD, Vc, and the AsA-GSH cycle to disseminate H2O2 and maintain healthy metabolism, high Cd stress caused Cd accumulation in the stem and leaves of S. fusiforme seedlings. The excessive Cd significantly restricted photosynthesis and reduced photosynthetic pigments in the seedlings, resulting in growth inhibition and deep morphological color, especially of the stems. High levels of Cd in seawater had toxic effects on commercial S. fusiforme seedlings, and risked this edible seaweed for human food.

... In addition, it appears from Table 1 that biosorption of Cd 2þ by microalgal-bacterial granules occurred, e.g. the cadmium content in microalgal-bacterial granules reached 2.42 ± 0.09 mg/g VSS after 24-day operation at the Cd 2þ concentration of 5 mg/L, and 3.66 ± 0.14 mg/g VSS after 16-day operation at 10 mg/L of Cd 2þ . In fact, it should be realized that biosorption of soluble heavy metals is a very common phenomenon, and the underlying mechanisms may include physisorption, chelation, complexation etc (Li et al., 2019;Souza et al., 2012). ...

So far, the microalgal-bacterial granular sludge process has attracted growing interest as an emerging wastewater treatment technology. Cadmium ion (Cd²⁺) commonly found in wastewater is toxic to microorganisms, thus its effect on microalgal-bacterial granules was investigated in this study. Results showed that Cd²⁺ at the concentration above 1 mg/L could compromise the performances of microalgal-bacterial granules. The removal efficiency of chemical oxygen demand decreased from about 70% in the control to 42.2% and 25.0% after 30-day operation at the respective Cd²⁺ concentrations of 5 and 10 mg/L, while the ammonia-nitrogen removal also declined from 70.4% to 30.5% with the increase of the Cd²⁺ concentration from 1 to 10 mg/L, indicating that nitrifying bacteria were susceptive to the presence of Cd²⁺. It was further revealed that Cd²⁺ could stimulate the production of extracellular polymeric substances, e.g. 190.19 ± 7.04 mg/g VSS in the presence of 10 mg/L of Cd²⁺ versus 100.26 ± 3.82 mg/g VSS in the control after 10-day operation. More importantly, about 84.1%–94.8% of Cd²⁺ was found to bind to the extracellular proteins in microalgal-bacterial granules at the Cd²⁺ concentrations studied. In addition, Chlorococcum and Cyanobacteria in microalgal-bacteria granules were withered in the presence of 10 mg/L of Cd²⁺, suggesting uncoupled symbiosis between microalgae and bacteria induced by Cd²⁺. Consequently, this study showed that Cd²⁺ could negatively impact on the microbial structures and metabolisms of microalgal-bacterial granular sludge, leading to a compromised process performance in terms of organic and nitrogen removal.

... (Acién et al. (2016)) assessed the practicability and importance of the use of microalgae for urban wastewater treatment. (Souza et al. (2012)) reviewed extensively the use of algae for the removal of cadmium and lead through bioremediation of wastewater. (Abdel-raouf et al. (2012)) summarized the various phases in the wastewater treatment of agricultural, domestic, and industrial wastes. ...

Heavy metals in the effluents released from industrial establishments pose risks to the environment and society. Prevalent organisms such as microalgae in industrial wastes can thrive in this harmful environment. The connection of the metal-binding proteins of the microalgal cell wall to the metal ions of the heavy metals enables microalgae as an ideal medium for biosorption. The current literature lacks the review of various microalgae used as biosorption of heavy metals from industrial effluents. This work aims to comprehensively review the literature on the use of microalgae as a biosorption for heavy metals. The study summarizes the application of different microalgae for heavy metals removal by identifying the various factors affecting the biosorption performance. Approaches to quantifying the heavy metals concentration are outlined. The methods of microalgae to generate biocompounds to enable biosorption of heavy metals are itemized. The study also aims to identify the materials produced by microalgae to facilitate biosorption. The industrial sectors with the potential benefit from the adoption of microalgal biosorption of heavy metals are recognized. Moreover, the current challenges and future perspectives of microalgal biosorption are discussed.

... Micro and macro algae play very important role in removal of heavy metals and organic contaminates due to their unique properties [172]. Baumann, Morrison, and Stengel [173], reported that accumulation of heavy metals affect the photosynthetic ability of macro alga. ...

Objectives To review red algae bioactive compounds and their pharmaceutical applications. Content Seaweed sources are becoming attractive to be used in health and therapeutics. Among these red algae is the largest group containing bioactive compounds utilized in cosmetic, pharmaceutical, food industry, manure and various supplements in food formula. Various significant bioactive compounds such as polysaccharides (aginate, agar, and carrageenan), lipids and polyphenols, steroids, glycosides, flavanoids, tannins, saponins, alkaloids, triterpenoids, antheraquinones and cardiac glycosides have been reported in red algae. The red algae have rich nutritional components Different polysaccharides of red algae possess the antiviral potential namely agarans, carrageenan, alginate, fucan, laminaran and naviculan. Sulfated polysaccharides and carraginans of red algae are rich source of soluble fibers which can account for antitumor activities depending upon chemistry of various secondary metabolites and metabolism of cell line. Flavons-3-ols containing catechins from many red algae block the telomerase activity in colon cancer cells. Contraceptive agents were tested from red algae as a source for post-coital. Lectin of red algae showed pro-healing properties and anti-ulcerogenic activities. Carragenates from red algae also conferred a positive influence on diabetes. Red algae depicted a reducing effect on plasma lipids and obesity. Porphyran from red alga can act as anti-hyperlipidemic agent also reduces the apolipoprotein B100 via suppression of lipid synthesis in human liver. Summary The polyphenolic extracts of Laurencia undulate, Melanothamnus afaqhusainii and Solieria robusta extract show anti-inflammatory effects against multiple genera of devastating fungi. Antioxidants such as phlorotannins, ascorbic acids, tocopherols, carotenoids from red algae showed toxicity on some cancer cells without side effects. Red algae Laurencia nipponica was found insecticidal against mosquito larvae. Red algae fibers are very important in laxative and purgative activities. Gracilaria tenuistipitat resisted in agricultural lands polluted with cadmium and copper. Outlook In the recent decades biotechnological applications of red algae has been increased. Polysaccharides derived from red algae are important tool for formulation of drugs delivery system via nanotechnology.

• Paulkumar Kanniah
• Parvathiraja Chelliah
• Jesi Reeta Thangapandi
• Sivasubramaniam Sudhakar

The green synthesis of metal and metal oxide nanoparticles (NPs) is one of the hot core topics and nanotechnology's great limelight. The green synthesis protocol is an excellent alternative and biologically malleable to other classical methods. The bio/green synthesized NPs gained significant attention due to remarkable optical, catalytic, and biological properties. Hence, in the past 10 decades, these bio/green NPs potentially showed the importance in various fields, including medicine, agriculture, catalysis, sensors, cosmetics, pharmaceuticals, and food technology. Therefore, in this chapter, we especially focused on the bio-ecofriendly synthesis of metal and metal oxide NPs using phytomolecules rich algae. Compared to microbe mediated NPs synthesis, the algae are environmentally amenable and compatible with the production of metal and metal oxide NPs. Both microalgae and macroalgae are the proficient biological sources serving its potential reduction and stabilization process on NPs production. Additionally, the possible mechanism involved during the NPs synthesis is also explained in detail. In the future, the NPs synthesized by algal extract could substantially occupy all the fields by exploring novel humanity products for our next generation.

• Fatma Abdelghaffar Afify

Dyes are associated with plenty of industrial and trade sectors. The discharge of dyes residues, including various chemical structures such as metal-complex, azo, diazo, and anthraquinone dyes, into the natural water bodies, creates adverse and non-aesthetics impacts on the aquatic ecosystem, as well as on humane healthful. The main challenge for these industries is to remove residues of dyes from dye-containing wastewaters to protect aquatic organisms and the environment from pollution. Moreover, the reuse of manipulated wastewater could effectively relieve freshwater resource deficiency. In this chapter, we review intelligent strategies to remove dyes that include taking advantage of the bio-resources using biological techniques to degrade and remove dyes from wastewater, such as microorganisms: yeast, fungi, and algae biomass. Also, the chapter discusses the role of the microorganisms in the removal of dyes from industrial wastewater focusing on the performance of the algae biomass that is an available bio-resource for biodegradation and biosorption of dyes-containing wastewaters.

Microalgae are aquatic photosynthetic organisms accomplished with an ability to differentiate between essential and nonessential metal ions for their growth. This selective approach makes them the most suitable candidate for heavy metal removal from contaminated wastewaters. The different detoxification mechanisms executed by microalgae involve biosorption and bioaccumulation. With particular emphasis on bioaccumulation, the present chapter highlights the role of metallothionein and phytochelatins in heavy metal detoxification. These peptides are synthesized to chelate heavy metal ions and assist compartmentalization of this peptide—metal complex in cell organelles of microalgae. The present chapter covers the biosynthesis and regulation of metallothionein/phytochelatins in microalgae as a response to different heavy metals. The application of an individual or integrated omics approach revealing the detoxification mechanism in microalgae is also reviewed. In a nutshell, the chapter will provide a comprehensive understanding of the adaptive mechanism of this scintillating microorganism for mitigating heavy metals in order of priority to clean the environment.

• Priyanka Sarkar
• Apurba Dey

Treatment of dye-containing wastewater is a major challenge for mankind that has gained much interest from the scientific community owing to the growing concerns of environmental safety and legislations. Thus, it becomes imperative to explore green and self-sustainable dye abatement methods. Phycoremediation is emerging as a new age technology with the goal of decolorization and detoxification of the hazardous dye laden effluents. The underlying mechanisms of phycoremediation of dyes are biodegradation, biosorption, and biocoagulation, which are influenced by several physicochemical and biological factors such as pH, temperature, contact time, surface characteristics, concentration and particle size of the algal biomass, chemical composition and concentration of the dye. This review provides a comprehensive insight into the potential, performance, and applications of phycoremediation methods in terms of the mechanisms, major determinants of phycoremediation processes, physical and chemical pretreatment methods of the algal biomass, and their effects on dye removal. The present article also discusses the emerging aspects of phycoremediation such as immobilization of algae, algal nanoparticles, activated carbon, and algal microbial fuel cell (A-MFC) for dye remediation along with the research gaps and future prospects. It was concluded from the literature review that immobilized algae and algal biochar exhibit enhanced dye uptake capacity due to improved porosity and surface characteristics. A-MFC can be used for simultaneous wastewater treatment and electricity generation. Furthermore, the generation of value-added products from algal biomass used in wastewater treatment has the potential for waste to wealth creation resulting in the improvement in economic feasibilities of the treatment process.

The Seaweed, Gracilaria edulis, collected from Mandapam coast, was studied for Biochemicalcharacterization of protein. Aqueous and methanol extracts yielded a total amount of 6.3 and 5.7 from 500 gof seaweed respectively. Crude protein extracts from the seaweed was 1.9 mg/mL in aqueous and 2.7 mg/mLin methanol extract respectively. The partial purification of protein is done by using DEAE cellulose. Theaqueous and methanol extracts showed highest antioxidant activity in DPPH (95 and 82%). On SDS-PAGE thecrude protein yielded four well defined bands at 31.4, 69.5, 92.7 kDa in both the extracts. The Fatty acid profileshowed that myristic acid was dominant in chloroform extract and palmitic acid was dominant in aqueousextract.

Forty-six strains of microalgae from BIOTECH Culture Collection (NSTDA), Microbiological Resources Center (TISTR) and Institute of Research and Food Development, 3 strains collected from Thai natural and industrial areas and 3 strains from the Gottingen University culture collection were tested for Mercury (Hg), Cadmium (Cd) and Lead (Pb) removal in aqueous solutions. In green algae, the highest Hg removal was by Scenedesmus sp., Chlorococcum sp., Chlorella vulgaris var. vulgaris and Fischerella sp., (97%, 96%, 94% and 92%, respectively). In blue green algae, highest Hg removal was by Lyngbya spiralis, Tolypothirx tenuis, Stigonema sp., Phormidium molle (96%, 94%, 94% and 93%, respectively). For Cd removal in green algae, the highest was by Chlorococcum sp., T5, Fischerella sp., Chlorella vulgaris var. vulgaris and Scenedesmus acutus (94%, 94%, 91%, 89% and 88%, respectively). In blue green algae, highest Cd removal was by Lyngbya heironymusii, Gloeocapsa sp., Phormidium molle, Oscillatoria jasorvensis and Nostoc sp. (97%, 96%, 95%, 94% and 94%, respectively). In green algae, highest Pb removal was by Scenedesmus acutus, Chlorella vulgaris var. vulgaris, Chlorella vulgaris, Scenedesmus vacuolatus and Chlorella vulgaris, (89%, 88%, 85%, 85% and 84%, respectively). In blue green algae, highest Pb removal was by Nostoc punciforme, Oscillatoria agardhii, Gloeocapsa sp., Nostoc piscinale, Nostoc commune and Nostoc paludosum (98%, 96%, 96%, 94%, 94% and 92%, respectively). Scenedesmus acutus had the highest concentration factor (CF) at 3,412, 4,591 and 4,078 for Hg, Cd and Pb, respectively. Tolypothrix tenuis had the highest maximum adsorption capacity of 27 mg Hg/g dry wt. at a minimum concentration of 1.04 mg/l, Scenedesmus acutus had the highest maximum adsorption capacity of 110 mg Cd/g dry wt. at a minimum concentration of 48 mg/l and Chlorella vulgaris had the highest maximum adsorption capacity of 127 mg Pb/g dry wt. at a minimum concentration of 130 mg/l.

This review covers the literature published in 2004 for marine natural products, with 693 citations (491 for the period January to December 2004) referring to compounds isolated from marine microorganisms and phytoplankton, green algae, brown algae, red algae, sponges, coelenterates, bryozoans, molluscs, tunicates and echinoderms. The emphasis is on new compounds (716 for 2004), together with their relevant biological activities, source organisms and country of origin. Biosynthetic studies (8), and syntheses (80), including those that lead to the revision of structures or stereochemistries, have been included.

• Eugenia Olguin

Phycoremediation applied to the removal of nutrients from animal wastewater and other high organic content wastewater is a field with a great potential and demand considering that surface and underground water bodies in several regions of the world are suffering of eutrophication. However, the development of more efficient nutrient removal algal systems requires further research in key areas. Algae growth rate controls directly and indirectly the nitrogen and phosphorus removal efficiency. Thus, maximum algae productivity is required for effective nutrient removal and must be considered as a key area of research. Likewise, low harvesting costs are also required for a cost-effective nutrient removal system. The use of filamentous microalgae with a high autoflocculation capacity and the use of immobilized cells have been investigated in this respect. Another key area of research is the use of algae strains with special attributes such as tolerance to extreme temperature, chemical composition with predominance of high added value products, a quick sedimentation behavior, or a capacity for growing mixotrophically. Finally, to combine most of the achievements from key areas and to design integrated recycling systems (IRS) should be an ultimate and rewarding goal.

In order to survive in a highly competitive environment, freshwater or marine algae have to develop defense strategies that result in a tremendous diversity of compounds from different metabolic pathways. Recent trends in drug research from natural sources have shown that algae are promising organisms to furnish novel biochemically active compounds. The current review describes the main substances biosynthesized by algae with potential economic impact in food science, pharmaceutical industry and public health. Emphasis is given to fatty acids, steroids, carotenoids, polysaccharides, lectins, mycosporine-like amino acids, halogenated compounds, polyketides and toxins.

Source: https://www.researchgate.net/publication/262664529_Algae_of_economic_importance_that_accumulate_cadmium_and_lead_A_review

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