Chekourn-et-al

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International Research Journal of Public and Environmental Health Vol.1 (2), pp. 19-32,April 2014 Available online at http://wendang.chazidian.com/irjpeh/

© 2014 Journal Issues ISSN 2360-8803

Original Research Paper

The role of algae in bioremediation of organic pollutants

Accepted 10 March, 2014

Kaoutar Ben Chekroun*1, Esteban Sánchez2 and Mourad Baghour1

1Department of Biology,

Observatoire de la Lagune de Marchica de Nador et Région Limitrophes (OLMAN-RL), Faculté Pluridisciplinaire de Nador, B.P. 300, 62700 Séloune, Nador, Morocco. 2Centro de Investigación en Alimentación y Desarrollo, A.C.Unidad Delicias -"Tecnología de

Productos Hortofrutícolas y Lácteos"Av. Cuarta Sur 3820, Fraccionamiento Vencedores del Desierto Cd. Delicias, Chihuahua.

México.C.P. 33089

The accumulation of organic pollutants in the environment can cause serious problems, affecting negatively the stability of many aquatic ecosystems and can also cause adverse effects to human health and the environment. Organic pollutants are introduced into the aquatic ecosystems as a result of human activities involving agricultural uses, fuel use and industrial discharges, domestic effluents and agricultural runoff. The persistent organic pollutants are toxic substances for environment and human health. Recently, there has been increasing interest on using bacteria, fungi, plants and algae to remove, degrade, or render harmless organic pollutants in aquatic systems. The algae play an important role in controlling and biomonitoring of organic pollutants in aquatic ecosystems. The use of higher plants and bacteria for bioextraction and bioremediation of heavy metals and organic pollutants have been extensively studied. However, the application of microalgae in restoration of organic-polluted aquatic environment has just started. In this review we present an overview of the potential of microalgae species for phytoremediation of organic pollutants in aquatic ecosystems.

Email : mbaghour@http://wendang.chazidian.com

Tel.:+212536358941 Fax. +212536609147

*Corresponding Author’s

Key words: Algae, bioremediation, organic pollutants, biodegradation

INTRODUCTION

The organic pollutants introduced into the environment through industrial discharges, agricultural uses, or improper waste disposal practices. The persistence of these chemicals in the environment poses a chronic threat to the health and safety of human and wildlife (Pavlostathis et al. 2001). Chemical contaminants present in the aquatic ecosystem may be immobilized and accumulated in sediments or may be subject to transformation and activation processes (Martínez-Jerónimo et al., 2008). Depending on biogeochemical processes, many organic pollutants like hydrocarbons are involved in adsorption, desorption and transformation processes and can be made available to benthic organisms as well as organisms in the water column through the sediment–water interface (Perelo 2010).

Hydrocarbons can become dangerous especially if they enter the food-chain, since several of the more persistent compounds, as PAHs and PCBs are carcinogenic (IARC 1983). According to the Stockholm Convention on

Persistent Organic Pollutants, 9 of the 21 persistent organic chemicals are pesticides. Classes of organic pesticides include organochlorine, organophosphate, organometallic, pyrethroids, and carbamates among others (Gilden et al. 2010, Stockholm convention 2011).

Relatively recently, there has been increasing interest on the use of bioremediation as the most desirable technology which uses plants (Phytoremediation) for removal of environmental pollutants or detoxification to make them harmless (Cunningham and Berti 1993). Methods for phytoremediation of contaminated soils, rivers and lakes are described in several reviews (Brooks 1998, Chaney et al. 1997, McIntyre and Lewis 1997, Flathman and Lanza 1998; Salt et al., 1998). Investigation on organic xenobiotics bioaccumulation/biodegradation in green algae is of great importance from environmental point of view because widespread distribution of these compounds in agricultural areas has become one of the major problems in aquatic ecosystem (Jin et al. 2012). The algae proved to be effective

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Int. Res. J. Public Environ. Health 20

in hyperaccumulation of heavy metals as well as degradation of xenobiotics (Suresh and Ravishankar 2004). In recent years, the use of microalgae in bioremediation of colored wastewater has attracted great interest due to their central role in carbon dioxide fixation. In addition, the algae biomass generated has great potential as feedstock for biofuel production (Huang et al. 2010). These bioremediation capabilities of microalgae are useful for environmental sustainability (Ellis et al. 2012, Lim et al. 2010).

Worldwide, trees, grasses, herbs, and associated fungi and microorganisms are being used increasingly for cleaning polluted sites. Phytoremediation is "on the brink of commercialization" (Watanabe 1997), and is given a rapidly increasing market potential (Flathman and Lanza 1998). The phytoremediation market is still emerging in Europe, while in the US revenues are likely to exceed $300 million in 2007 (Campos et al. 2008). In a recent study (Yamamoto et al. 2008), benthic microalgae have been used for the first time in the remediation of organically enriched sediments.

This review aims to give an overview over mechanisms used by microalgae for bioremediation of organic pollutants in aquatic ecosystems and the impact of genetically modified microalgae on xenobiotic degradation to minimize their impact on the environment.

Bioremediation of petroleum hydrocarbons

The accumulation of petroleum hydrocarbons in the environment can cause serious problems, affecting negatively the stability of many aquatic ecosystems and can also cause difficulties for animals and human health. The amount of natural crude-oil seepage is currently estimated to be 600,000 metric tons per year, with a range of uncertainty of 200,000 to 2,000,000 metric tons per year (Kvenvolden and Cooper 2003).

The bioremediation technology offers a promising tool to treat aerobically oil-contaminated shorelines (Atlas 1991, Rosenberg et al. 1992, Venosa et al. 1992). This technique of decontamination of polluted areas gives much hope on the restoration of polluted mangrove swamps and is being utilized for the degradation of crude oil in soil matrix by using microorganisms, to transform the petroleum hydrocarbons into less toxic compounds (Davies and Westlake 1979, Orji et al. 2012a). This is achieved by the help of bacteria, fungi, algae that produce enzymes capable of degrading harmful organic compounds (Davies and Westlake 1979). In the presence of abundant hydrocarbon in the environment after a spill, microorganisms cannot effectively attack and utilise the hydrocarbon unless limiting nutrients such as nitrate, phosphate, even micro-elements are incorporated into the polluted medium (Van Hamme et al. 2003).

Microalgae and protozoa are the important members of the microbial community in both aquatic and terrestrial

ecosystems however only few reports are available regarding their involvement in hydrocarbon biodegradation (Jain and Bajpai 2012). On the other hand, introduction of hydrocarbon degrading bacteria in oil contaminated sites does not guarantee to remove all components of crude oil because some components still remain difficult to degrade, such as alkanes of shorter and longer chains (<C10 and C20–C40) and polycyclic aromatic hydrocarbons (PAHs) (Yuste et al. 2000). Several microorganisms can metabolise the nonchlorinated aliphatic and aromatic hydrocarbons as sources of carbon, but due to their hydrophobicity they pass very slowly to the aqueous phase liquid where microorganisms are active (Brusseau 1998). Recently Orji et al. (2012b) reported that the Remediation by Enhanced Natural Attenuation (RENA) is currently being used as a cleanup technology in polluted environments with petroleum hydrocarbon in the Niger Delta including mangrove ecosystems. RENA is a full-scale bioremediation technology in which contaminated soils, sediments and sludge’s, are periodically turned over or tilled into the soil to aerate the waste. This technique involves factors such as evaporation, dispersion, spreading, dissolution, oxidation, emulsification and spreading.

The asphaltenes (Figure 1), the most complex hydrocarbons of the petroleum, contain nitrogen, sulphur and oxygen (Mitra-Kirtley et al., 1993), and are very resistant to the microbial degradation (Guiliano et al. 2000). Pineda-Flores et al. (2001) found that a microbial consortium isolated from crude oil was able to take faster and greater oxygen consumption when it was mixed to asphaltenes as the only source of carbon and energy, and is able to degrade the crude oil too. Some microalgae produce enzymes capable of degrading harmful organic compounds to transform the petroleum hydrocarbons into less toxic compounds (Davies and Westlake 1979).

The microalgae Scenedesmus obliquus GH2 (Table 1), is used to construct an artificial microalgal-bacterial consortium for crude-oil degradation (Tang et al. 2010). Addition of the bacterial consortium in different amendments significantly enhanced degradation efficiency of both aliphatic and aromatic hydrocarbons of crude oil. Another consortium of pre-isolated oil-degrading bacteria in association with three species of plants effectively remediated contaminated silt-loam soil more than silt, loam and sandy loam with an average 80% reduction of total petroleum hydrocarbon (Ghosh and Syed 2001).

The presence of the Rhodococcus genus, which has been associated with the biodegradation of n-alkanes up to C36, and the high content of heavy alkanes in the Prestige fuel could indicate that Rhodococcus has a role in the degradation of fuel (Jiménez et al. 2007).

Bioremediation of polychlorinated biphenyls (PCBs)

Polychlorinated biphenyls, PCBs (Figure 2), are among the

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Chekroun et al. 21

: Chemical structure of Asphaltenes from traditional heavy crudes

Table 1: Organic pollutants accumulation by algal species and Pseudomonas migulae Phytoplankton

fusiformis

Amphora coffeaeformis

phenanthrene, pyrene pyrimethanil) and herbicide

(isoproturon).

chlorinated hydrocarbons Harding and Phillips 1978

worst pollutants because of their toxicity, carcinogenicity, wide distribution and slow biodegradation in the environment (Perelo 2010, Meagher 2000). Some monohydroxylated PCBs are potent endocrine disrupters (Figure 1C), and some PCB metabolites with a hydroxy group in the meta or para position have been reported to be involved in developmental neurotoxicity (Maltseva et al. 1999).

PCBs were used extensively in a variety of industrial

applications due to their thermal stability and persist in aquatic sediments (Dhankher et al. 2012). Some microorganisms can degrade PCBs aerobically or anaerobically under a variety of conditions (Borja et al. 1999, Pieper and Seeger 2008). PCB degradation is complex as there are many different forms and it has been shown that orthochlorinated PCBs inhibit and inactivate a key enzyme in the degradation pathway, dehydroxybiphenyl oxygenase (Dai et al. 2002). Aerobic

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Int. Res. J. Public Environ. Health 22

Figure 2:Structures of PCBs (numbers 2-6 (2’-6’) indicate the possible positions of the chlorine atoms at ortho(o), meta(m) and para(p) positions)

Figure 3: Stephanodiscus minutulus according to Cruces et al. (2010)

degradation of lower chlorinated PCBs is via co-metabolism by dioxygenases, resulting in ring cleavage and possibly complete mineralization (Dhankher et al., 2012).

Phytoplankton plays a critical role in controlling the fate of persistent organic pollutants (POPs), such as PCBs in the water column because they are high in lipids and they serve as the base of both the pelagic and benthic food chains (Lynn et al., 2007).

Benthic microalgae have been used for the first time for in situ remediation of the organically enriched sediments (Yamamoto et al. 2008). Previously Harding and Phillips (1978) suggested that marine organisms including phytoplankton can uptake and accumulate several chlorinated hydrocarbons decreasing their concentrations in the media. Lynn et al. (2007) analysed the effect of different nutrient treatments on the uptake of PCB

congener 2,2',6,6'-tetrachlorobiphenyl by the diatom Stephanodiscus minutulus (Figure 3) and transfer to a zooplankton (Daphnia pulicaria), and they found that the uptake of PCB by phytoplankton can be significantly altered by nutrient availability which subsequently affects transfer to zooplankton, potentially through such responses as grazing rate and lipid assimilation.

The association of PCBs and live algal cells in rivers was studied by Fitzgerald and Steuer (2006), suggesting a positive relations between particle-associated PCBs and both chlorophyll-a and algal carbon concentrations indicated that live algal cells were a significant sorption phase for dissolved PCBs.

Previously Lara et al. (1989) reported the ability of brown algae Caepidium antarcticum and Desmarestia sp. to associate their exudates with hydrophobic pollutants such

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Chekroun et al. 23

Figure 4. The degradation pathway of Phenanthrene, a PAH compound by the cyanobacteria Agmenellum quadruplicatum PR-6 (Narro et al. 1992).

as polychlorinated biphenyls (PCBs). Organic macromolecules in seawater samples and exudates from brown algae Ascophyllum nodosum and Fucus sp. are able to incorporate organic compounds like amino acids, sugars and fatty acids. PCBs are generally deposited in the lipid stores of organisms and Berglund et al. (2001) found that lipid content explained most of the variation of PCB concentration in phytoplankton in 19 southern Swedish lakes.

Recently Chun et al. (2013) reported that a common limitation is the lack of an effective method of providing electron donors and acceptors to promote in situ PCB biodegradation, and the application of an electric potential to soil/sediment could be an effective means of providing electron-donors/-acceptors to PCB dechlorinating and degrading microorganisms, suggesting that this approach could be a cost-effective, environmentally sustainable strategy to remediate PCBs in situ.

Bioremediation of polycyclic aromatic hydrocarbons (PAHs)

Polycyclic aromatic hydrocarbons, PAHs, are ubiquitous pollutants in aquatic ecosystems (Figure 4). PAHs naturally occur in fossil fuels such as coal and petroleum, but are also formed during the incomplete combustion of organic materials such as coal, diesel, wood and vegetation

(Freeman and Cattell 1990, Lim et al. 1999). PAHs are a class of organic compounds that consist of two or more fused benzene rings and/or pentacyclic molecules that are arranged in various structural configurations (Bamforth and Singleton 2005). They are highly recalcitrant molecules that can persist in the environment due to their hydrophobicity and low water solubility (Cerniglia 1992). PAHs are produced primarily during fuel combustion and share many properties with PCBs: elevated boiling points, very low solubility in water, high stability and toxicity (Lima et al. 2005).

The phytoremediation of PAHs have limited success due to the high toxicity of this class of pollutants (Dhankher et al. 2012). The accumulation and biodegradation of two typical polycyclic aromatic hydrocarbons (PAHs), phenanthrene (PHE) and fluoranthene (FLA), by the diatoms was studied by Hong et al. (2008), using two algal species Skeletonema costatum (Figure 5) and Nitzschia sp (Figure 4). The authors found that the accumulation and degradation abilities of Nitzschia sp. were higher than those of S. costatum. Degradation of FLA by the two algal species was slower, indicating that FLA was a more recalcitrant PAH compound. The microalgal species also showed comparable or higher efficiency in the removal of the PHE-FLA mixture compared with PHE or FLA alone, suggesting that the presence of one PAH stimulated the degradation of the other.