CC BY
86
Journal of Stress Physiology & Biochemistry, Vol. 15, No. 4, 2019, pp. 53-67 ISSN 1997-0838 Original Text Copyright © 2019 by Basel Saleh
ORIGINAL ARTICLE
OPEN /71 ACCESS
Algae Efficacy as a Potent Tool for Heavy Metals Removal: An Overview
Basel Saleh
Department of Department of Molecular Biology and Biotechnology, Atomic Energy Commission of Syria, P.O. Box 6091, Damascus, Syria
*E-Mail: ascientific@aec. orq.sy
Received October 14, 2019
Water pollution with heavy metals sharply increased worldwide and became a serious problem a cause to expansion industrial activities worldwide. Pollutants caused deleterious effect on living organisms in ecosystems. Thereby, various physico-chemical and biological methods were employed for overcoming this problem. Algae (micro and macrophyla) among biological systems displayed multiuse applications in food and industry. Of which they exhibited a significant and important role as a useful tool in heavy metals removal capacity. Algae as renewable resources, their abundance worldwide and ability to concentrate heavy metals in their tissues, encouraged scientists to focusing on their implementation in heavy metal pollutants reduction from environmental ecosystems. Their efficacy and advantageous over physico-chemical methods make them as alternative, eco-sustainableand potent way for heavy metals removal.
Key words: Algae, Biosystem, Biosorption, Heavy metals, Pollutants, Removal capacity
From very long time up till now, environmental pollution by heavy metals was considered as a global public health concern and has been dramatically increased due to their exponentially increased used for various purposes like e.g. industrial, agricultural, domestic and technological applications (Bradl, 2002; Nazal, 2019).
Wastewater (municipal and industrial) is any water type negatively affected in quality due anthropogenic influence. Wherein, nickel, lead, chromium, cadmium, zinc and iron were the most toxicant elements against all living organisms' life (Jamers et al., 2013; Saleh, 2017a).
Effluents of factories can be used for irrigation purpose worldwide. However, these effluents have different harmful materials needed treatment before using for irrigation or other purposes. Green technology based upon algae biomass seems to be a good and alternative way for bioremediation. This tool has been investigated too earlier over the past 40 years by Ryther et al. (1972).
According to Kumari et al. (2006)"Bioremediation is a pollution control technology that uses biological systems to catalyze the degradation or transformation of various toxic chemicals to less harmful forms. It was considered as a cheaper and potent method and highly uses increasing for environmental pollution reduction. It has been documented that sewage disposal formed an ecological problem threatening urban and semi-urban countries. Moreover, the effluents from residential and industrial discharge is considered as a principal source of water pollution; where they discharged into open drains that finally joins the rivers (Kumari et al, 2006).
Heavy metal pollutants like lead, cadmium, mercury, arsenic, iron, nickel, copper, aluminium and zinc are considered as a major poisoning and toxicant environmental pollutants (Dias , 2002).Toxicant pollutants danger comes from their easily absorption and fast accumulation in low organisms and then transported to human through food chain (World, 1992; Pinto et al., 2004). Thereby, wastewater treatment to resolve this crisis is requested.
Different physico-chemical methods including
filtration, adsorption, chemical precipitation, ionexchange, phytoremediation etc. are integrated for removing heavy metals toxicity from wastewaters (Mehta and Gaur, 2001). The limitations occurred with physico-chemical methods such for example, their efficacy is limited for selective metals and not for all and very expensive tool (Fawzyaand Issa, 2016; Djati Utomo et al., 2016). Thereby, living organisms e.g.plant (Gupta and Sarine, 2009);bacteria (Iyer et al., 2005; Javanbakht et al., 2014), yeast (Goksungur et al., 2005), fungi (Anayuri et al., 2009; Javanbakht et al., 2014) and algae (Mallick and Rai, 1992; Lawton et al., 2013; Javanbakht et al., 2014; Jerold et al., 2016; Fawzya and Issa,2016; Ghazal et al.,2018; Bilal et al., 2018)are as alternative way to solve this problem with low cost. Among these biological systems, microalgae highly absorb nutrients because they require metals as micronutrients for their biological process and huge amounts of nitrogen and phosphorus for proteins synthetize (45-60% microalgae dry weight).
It has been demonstrated that algae (both live and dried biomass) can consider as a good biosorbents for heavy metals elimination and reduction form ecosystems. Over past year, population expansion and industrial activity caused freshwater quality deterioration through the world leading finally to freshwater shortages around some areas. In this regards, U.S. geological survey revealed that global water demand will exceed supply by 56% in 2025
(http://www.theworldwater.org/water_facts.php.).
This review will focus on application of algae (micro and macro) species used as a biological system for heavy metals removal. As known, algae taxonomy includes many criteria like colors (pigments), cell wall composition, flagella number and position, structure cellular, growth patterns, branching and sporangia types. Based upon the mentioned criteria, they divided into green algae (Chlorophyta), brown algae (Phaeophyta), red algae (Rhodophyta) (Wajahatullahet al., 2009; Bilal et al., 2017) and blue-green algae (Cyanophyta).
It has been demonstrated that since 1990 up till now, more than of 5000 publications regarding heavy metals bioadsorption, and that approximately 6% of these
reports have been focused on marine algae application (Nazal, 2019).
Reviewing of the literature published
Algae exhibited a critical role as a potent biosorbent of heavy metals and showed different removal capacity according to algae species, their density and form (live or dried biomass), heavy metal concentration and formula, pH of solution, their application in single or combined of more than one species and others (Bilal et al., 2018).
It has been documented that the request of wet seaweed for different purposes was approximately 8 million in 2003, 19 million tonnes in 2010 and 24 million tonnes in 2014. However, the world production of cultivated algae increased day by day worldwide in recent years and that this impressively augments particularly in Indonesia (FAO, 2014; McHugh, 2003).
Among biological systems, microorganisms implementation (particularly bacteria, fungi, yeasts and algae biomass) has received huge interest for heavy metal sorption due to their characteristic e.g. high surface to volume ratio; large availability, rapid kinetics of adsorption and desorption and low cost (Abbaset al., 2014).
Microalgae are highly biodiversity approximately between 200.000- several millions, of which less than 10,000 were described (Sharma and Rai, 2011). Delrue et al. (2016) reported that microalgae displayed high board range as pollutant scavengers (domestic, industrial and agricultural).
Earlier, Oswald and Gotaas (1957) reported utility of microalgae for wastewater in sewage treatment. Among them, Chlorella vulgaris, Neochloris oleoabundans, Scenedesmus dimorphous, Spirulina,
Nannochloroposis, Dunaliella salina and Botrycoccus braunii species were mainly used for wastewater treating (Chong et al., 2000).
Prabha et al. (2016) reviewed the utility of some algae used for wastewater treatment e.g.Chlorella vulgaris and Scenedesmus dimorphus (Ammonia NH3 and Phosphorous), Padina spp. and Cladophora fascicularis (Copper Cu), Spirulina and Spirogyra (Lead Pb), Chlorella vulgaris (Copper Cu, Cadmium Cd,Zinc Zn and Lead Pb), Scenedesmus obliquus (Cadmium
Cd), Sargassum sinicola (Cadmium Cd and Copper Cu) and Dunaliella (Mercury Hg, Cadmium Cd and Lead Pb).
Bayramoglu et al. (2006) reported that Chlamydomonas reinhardtii removal capacity was 89.5 mg/g, 66.5 mg/g and 253.6 mg/g for Hg, Cd and Pb heavy metals, respectively. Whereas, Kumar et al. (2015) reported the importance of Chlorella marina (Butcher) for removing of Chromium (Cr) and Lead (Pb) from waste waters.
Cheng et al. (2017) reported that Chlorella vulgaris removal capacity for Cd was recorded to be 95.2% and 96.8% with dead and live algae, respectively.
Wang et al. (2010) reported that Chlorella vulgaris microalgae capacity for removing phosphorus by more than 99%. Similarly, Salgueiro et al. (2016) reported efficacy of Chlorella vulgaris microalgae for removing phosphorus by more than 99% and the chemical oxygen demand (COD) by 71% from wastewater.
Kshirsagar (2013) reported the capacity of two microalgae Chlorella vulgaris for removal of nitrate and chemical oxygen demand (COD); whereas, Scenedesmus quadricauda showed best removal capacity for biochemical oxygen demand (BOD) and phosphate. In this respect, BOD reduction level was recorded to be 70.91 % and 89.21 % using C. vulgaris and S. quadricauda, respectively. Whereas, COD removal level was recorded to be 80.64% and 70.97% using C.vulgaris and S. quadricauda, respectively after over 15 days.
Great attention has been given to implementation of microalgae in bioremediation of colored wastewater due to their capital role in carbon dioxide fixation. In this regards, Singh et al. (2010) reported that the removal of color from textile dyes effluent mechanism could be realized either by biosorption or bioconversion. For example, the removal level of the color from the mono-azo dyes by conversion it into aniline ranged between 63 - 69% by Chlorella vulgaris.
Recently, Ghazal et al. (2018)reported removal capacity of five microalge (Anabaena flos aquae, Nostoc elepsosporum, Nostoc linkia, Anabaena variabilis and Chlorella vulgaris) for BOD and COD, after 4 weeks incubation. They reported that the removal BOD capacity was recorded to be 73.96, 98.92, 85.63,
82.00 and 92.24%; whereas, for COD it was recorded to be 60.00, 98.00, 75.00, 80.00 and 97.63% by A. flos aquae, N. elepsosporum, N. linkia, A. variabilis and C. vulgaris, respectively. Moreover, they reported that their capacity to remove some heavy metals. In this regards, the reduction level for Cr was 60.36, 99.19, 67.31, 97.57 and 90.94%; whereas, for Pb it was 73.00, 98.80, 89.40, 94.00 and 96.40; while it was 46.67, 95.00, 69.33, 66.00 and 88.33% by A. flos aquae, N. elepsosporum, N. linkia, A. variabilis and C. vulgaris, respectively.
Previously, Hammouda et al. (1995) reported that a mix of Chlorella sp. and Scenedesmus sp. together could remove 90% of the COD of an urban wastewater (from 180 to less than 20 mgO2/L.
Vijayakumar and Manoharan (2012) reported increase in dissolved oxyge (DO) content and reduction BOD and COD up to 95% was observed using both Oscillatoria brevis and Westiellopsis prolifica in dye industry effluent.
Balaji et al., (2014) reported the potent role of several Spirulina strains (S. indica, S. maxima and S. platensis) for Zn and Ni biosorption.
Limaet al. (2004) reported removal p-chlorophenol level (10 mg/L/day) by Chlorella vulgaris and Coenochloris pyrenoidosa. Whereas, Papazi and Kotzabasis(2013) reported the capacity of Scenedesmus obliquusfor removing 3,4-dichlorophenol (6 ^mol/day); 2,3-dichlorophenoland 2,5-
dichlorophenol(9 ^mol/day); 2,4-dichlorophenol (10 ^mol/day) and 2,6-dichlorophenol (13 ^mol/day).
Penget al. (2014) reported the capacity of Scenedesmus obliquus for removing progesterone and norgestrel (0.3 ^mol/day); Chlorella pyrenoidosa for removing norgestrel (0.2 ^mol/day) and progesterone (0.3 ^mol/day). Wang et al. (2013) reported
Chlorella pyrenoidosa importance for removing triclosan by 104 mg/L/h. Whereas, De Godoset al. (2012) reported Chlorella vulgaris importance for tetracycline removing. While, Sethunathan et al. (2004) reported capacity of Chlorococcum sp. and Scenedesmus sp. for removing a-endosulfan by 0.135 mg/L/day and 0.140 mg/L/day, respectively. Kumar et al. (2015) reviewed of 63 bioremediation cases out of 265 microalgae-heavy metal couples (other cases are
adsorption experiments on dead cells with or without pretreatment) from 0.02 to 1378 mg/g. Ke et al. (2010) reported the importance of Selenastrum capricornutum for removing PAHs + heavy metals and they reported heavy metals positive effect on PAHs reduction.
Salgueiro et al. (2016) reported that the levels of phosphorous and COD decreased rapidly due to the fast assimilation by Chlorella Vulgaris microalgae in nine days of culture in wastewater. Some studies have demonstrated that this microalga can grow faster in presence of organic acids or glucose that function directly as essential organic nutrients (Wang et al., 2010).This indicates that microalgae could assimilate some organic compounds, resulting in a rapid drop of chemical oxygen demand concentration during the first days of the culture.
Tuzun et al. (2005) reported that Chlamydomonas reinhardtii capacity to remove Hg2+, Cd2+ and Pb2+ was approximately 98%. Whereas, Felisco and Billacura (2018) reported microalgae Nannochloropsis oculata capacity for Pb removal from industrial wastewater.
Blue-green algae ( Cyanophyta) were also considered as potent tools for heavy metals removal. In this regards, El-Enany and Issa (2000) reported that Nostoc linckia could be consider as tolerant to heavy metals (Zn and Cd) and is able to accumulatethese metals.
Whereas, Rai and Tripathi (2007) reported blue -green alga Microcystis removal capacity for chromium (VI), cadmium (II) and copper (II) in single or in combination. They reported the importance of Microcystis as eco-sustainable approach to remove the mentioned metals. Moreover, Gelagutashvili (2013) reported cadmium (Cd), chromium (Cr), silver (Ag) and gold (Au) removal by cyanobacteria Spirulina platensis, Streptomyces spp. and Arthrobacter species living and non-living cells, from aqueous solution. The previous study reported thatcyanobacteria capacity to remove the mentioned metals depend on cyanobacteria type and uptake conditions. Whereas, Goswamiet al. (2015) reported that Nostoc muscorum removal capacity was 66% for Zn and 71% for Cu. Indeed, Shilpi et al. (2015) reviewed cyanobacteria potent for heavy metals removal. Indeed, Fawzya and Issa(2016) reported that
Cyanosarcina Fontana showed high heavy metals accumulation of Fe2+(93.95%), Pb2+ (81.21%), Cu2+ (63.9%), and Mn2+ (48.49%)from sewage plant compared to Anabaena oryzae.
Overall, microalgae frequently used for chemical pollutants removal are summarized in Table 1.
As for macroalgae, they were accounted to be approximately 9000 macroalgae species around the oceans worldwide (Wajahatullah et al., 2009; Saleh and Al-Mariri, 2017). It has been demonstrated that macroalgae showed different affinities towards the same metal depend upon the macroalgae chemical structure (Volesky 2003).
It has been reported that Spirogyra sp. capacity to remove Cr was 14.7 mg/g d.m (Gupta et al., 2001); Spirogyra sp. capacity to remove Pb was 140 mg/g d.m (Gupta and Rostogi 2008a) and Spirogyra sp. to remove Cu was 133.3 mg/g d.m (Gupta et al., 2006).
Feng et al. (2004) reported that Ecklonia maxima metal sorption capacity was 85-94, 227-243 and 83.5 mg/g d.m for Cu, Pb and Cd, respectively. Indeed, Gupta and Rostogi (2008b) reported that Oedogonium sp. capacity removal of Pb was recoded to be 145 mg/g d.m.
Ulva lactucaamong chlorophyta was used as a potential tool for bioremediation of reject water(Robertson-Andersson et al., 2008; Nielsen et al., 2012; Sodeet al., 2013), and other Ulva spp.(Lawton et al., 2013).Asnaoui et al. (2014) reported U. lactuca capacity for removing chromium (Cr) form solution. The previous study showed that living organism capacity to remove Cr was 84 %and to be 96%for crushed algae.
Whereas, Ben Chekroun and Baghour (2008) reviewed the most algae species used for heavy metalsbioremediatione.g.Ascophyllum nodosum (Gold Au; Cobalt Co; Nickel Ni and Lead Pb), Caulerpa racemosa Boron (Br), Fucus vesiculosus (Zinc Zn and Nickel Ni), Sargassum fluitans (Copper Cu; Iron Fe; Zinc Zn and Nickel Ni), Sargassum natans and Sargassum vulgare Lead (Pb), Spirogyra hyalina Cadmium (Cd), Mercury (Hg), Lead (Pb), Arsenic (As) and Cobalt (Co).Moreover, Christobe and Lipton (2015) reported that the maximum arsenic removal capacity was 90.2% at biomass weight of 2g/100 ml for Sargassum wightii
(brown alga) and Gracilaria corticata (red alga).
Toxic metal removal from wastewater by Laminaria hyperboreabrown marine macroalgae according to matrix type and operating conditions has been reported by many reports; e.g (Zn2+=2.4-4.3 mg/L, Ni2+=2.2-4.2 mg/L and Cu2+=2.1-2.5 mg/L) (Cechinel et al. 2016); (Zn2+=18.1-21.5 mg/L) (Mazur et al. 2016). Whereas, Castro et al., (2017) reported Fucus vesiculosus brown marine macroalgae capacity for removing some metals (Zn2+=546.0 mg/L, total Cr=10.8 mg/L and total Fe=22.9 mg/L).
Sari and Tuzen (2008b) reported that red alga Ceramium virgatum removal capacity for Cd was recorded to be 39.7 mg/g.
Recently, Mazur et al. (2018) reviewed brown marine macroalgae as a potential tool for heavy metals removing from industrial wastewaters. Indeed, they discussed advantages and disadvantages of the different methods (chemical precipitation, coagulation/flocculation, membrane filtration, electrochemical processes, ion exchange, adsorption and biosorption) employed for removing heavy metals from wastewaters.
Djati Utomoet al. (2016) reported comparative study between marine algae (MA) and freshwater algae (FA) biomass for Cu, Pb, Cd and Zn heavy metals absorption. They reported that MA showed higher absorption capacity of the mentioned metals compared to FA once. In this regards, absorption capacity was 22%, 67%, 98%, 39% of Cd, Cu, Pb and Zn respectively, for MA. Whereas, it was 18%, 29%, 94%, 37% of Cd, Cu, Pb and Zn respectively for FA.
Ibrahim and Mutawie (2012) reported removal capacity of red algae Laurancia obtusa, Geldiella acerosa & Hypnea sp. for Cu, Zn, Mn & Ni. They reported that this capacity was 94%, 85% and 71% for L. obtusa, G. acerosa and Hypnea sp., respectively.
More recently, Nazal (2019) reviewed some macromarine algae (red, green, and brown) applied for heavy metals removal from aqueous solution.
It has been demonstrated that brown algae out macroalgae occupied an attractive position for heavy metals removal by showing the highest metal binding capacity (Ofer et al., 2003; Herrero et al., 2006).
Overall, macroalgae frequently used for chemical pollutants removal are summarized in Table 2.
As for aquatic plants, they exhibited a significant role in heavy metals biosorption. In this regards, Hydrilla verticillata and Ceratophyllum demersum aquatic plants were used to remove Cd, Hg and Cu heavy metals from aqueous solution (Gupta and Sarine 2009). Algal heavy metals biosorption mechanisms
Algae species developed various mechanisms defense against heavy metals. Anyway, it has been demonstrated that the mechanisms involved in pollutants biosorption are not clearly evident.
For microalge, different mechanisms of pollutants biosorption process by algae have been reported. In this respect, Ahluwalia and Goyal (2003) proposed that pollutants biosorption process consists of two steps. Firstly, metals ions bind and secondly, they accumulate on the binding sites.
Javanbakht et al. (2014) proposed that biosorption process of heavy metals by microorganisms includes the following mechanisms: transport across cell membrane, complexation, ion exchange, precipitation, and physical adsorption. Whereas, Rajfur (2013) reviewed sorption properties of marine and freshwater algae and the physicochemical factors impact on algal sorption properties. The previous review showed that temperature, pH, intensity of the photosynthetically active light and the presence of other ions and anions were the major abiotic factors affect metals sorption process.
As for cyanobacteria, El-Enany and Issa (2000) reported that Nostoc linckia cyanobacteria showed high tolerance to heavy metals (Zn and Cd) through adsorption them on the cell surface and/or due to sequestration them via metal-binding protein. Whereas, Shilpi et al. (2015) reviewed cyanobacteria potent for heavy metals removal in correlation to antioxidant enzymatic systems [superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX) and Glutathione reductase (GR)]. Similarly, different studies demonstrated their capacity to remove heavy metals related to the above antioxidant systems; e.g. Sultan et al. (2007) applied Anaebaena doliolum to remove Cd and Cu. Whereas, Singh et al. (2012) applied Anabaena
spto remove Cd. While, Zutshi et al. (2014) applied Hapalosiphon fontinalis to remove As. Moreover, Balaji et al., (2014) reported that Zn and Ni removal capacity by several Spirulina strains (S. indica, S. maxima and S. platensis) could be related to their content of different functional group (carboxyl, hydroxyl, sulfate and others) binding site with metals.
Moreover, macroalgae (seaweeds) among algae species were considered as a potent and good pollutants biosorbent due to their large surface area, highly poly-functional groups content on the metal-binding site (for both cationic and anionic complexes).
It has been demonstrated that metals accumulation and uptake capacity by algae biomass mainly depends on the polysaccharide (e.g. alginates and fucoidans) contents availability on the cell surface (Herrero et al., 2006). They reported that marine brown alga among different algae species, displayed an important role in pollutant biosorption due to their richness on polysaccharide.
Among these groups, carboxyl, amine, imidazole, phosphate, sulfate, sulydryl, and hydroxyl groups, as well as proteins and sugar molecules were mainly involved in biosorption process. In this respect, ligands of seaweeds were considered as an ionic interaction with metals in the aqeous solutions, forming a critical and major mechanism for binding (Yun et al., 2001).Tamilselvan et al. (2011) reported that carboxyl (-COOH), hydroxyl (-CHOH) and amine (-NH2) groups were the main functional groups involved in Cr, Pb, Cd and Hgbiosorption byAcanthophora spicifera algae using FT-IR. Whereas, Dekhil et al. (2011) reported that O-H bending, N-H stretching, C-N stretching, C-O and S=O stretching as functional groups detected in Pb(II) and Cd(II) ions sorption in the Caulerpa racemosa green alga using FT-IR.
Saleh (2015) reported biosorption of 4 heavy metals (Cu, Pb, Zn and Cd ions) from aqueous solution using green algae Ulva lactuca (Chlorophyta). The previous study revealed that the C-H, C=O, CH2 and C-O-C groups were mainly involved in heavy metals absorption based on fourier transform raman spectroscopy (FTRaman) technique. Moreover, Saleh (2017a) reported biosorption of the same above mentioned
pollutants by U. lactuca based on fourier transform infrared spectroscopy (FTIR) analysis. The previous study revealed that O-H, N-H, -C-O, P-O-C, S-O, C-C, -C-C, -C-OH, C-H and C-I groups were the main functional groups involved in pollutants biosorption processes.
Saleh (2017b) reported functional groups involved in Cd biosorption with Ulva lactuca (Chlorophyta) and Padina pavonica (Phaeophyta) seaweeds based on
fourier transform infrared spectroscopy (FTIR) analysis. The previous study revealed that carboxylic acids (C-O) & amides (C-N stretch) groups and aromatics groups (C-C stretch) were the mainly functional groups involved in Cd biosorption by U. lactuca green algae. Whereas, amides groups (C=O stretch), alcohols (O-H stretch) and phenols (H-bonded) were mainly involved in Cd biosorption process by P.pavonica brown algae.
Table 1.Microalgae used for chemical pollutants removal.
Green Chemical pollutants References
Chlorella marina Cr & Pb Kumar et al., (2015)
Chlorella marina Ammonia NH3 and Phosphorous Prabha et al., (2016)
Chlorella vulgaris Cu, Cd, Zn & Pb Prabha et al., (2016)
Chlorella pyrenoidosa&Scenedesmus obliquus Progesterone & norgestrel Peng et al., (2014)
Chlorella pyrenoidosa Triclosan Wang et al., (2013)
Chlorella vulgaris Tetracycline De Godos et al., (2012)
Chlorella vulgaris Phosphorus Wang et al.,(2010)
Chlorella vulgaris Phosphorus & COD Salgueiro et al., (2016)
Chlorella vulgaris& Scenedesmus quadricauda Nitrate, COD & BOD Kshirsagar (2013)
Chlorella vulgaris BOD & COD Ghazal et al., (2018)
Chlorella vulgaris Cd Cheng et al, (2017)
Mix of Chlorella sp. &Scenedesmus sp. COD Hammouda et al.,(1995)
Chlorella vulgaris and Coenochloris pyrenoidosa p-chlorophenol Lima et al., (2004)
Spirulina sp. (S. indica, S. maxima&S. platensis) Zn & Ni Balaji et al.,(2014)
Spirulina Pb Prabha et al., (2016)
Scenedesmus obliquus Cd Prabha et al., (2016)
Scenedesmus quadricauda Cd Mirghaffari et al, (2015)
Scenedesmus quadricauda Pb Mirghaffari et al, (2015)
Dunaliella sp. Hg, Cd & Pb Prabha et al., (2016)
Micrasterias denticulate Cd Ben Chekroun and Baghour (2008)
Scenedesmus obliquus 3,4-, 2,3-, 2,5- 2,4- and 2,6-dichlorophenol Papazi and Kotzabasis (2013)
Chlorococcum sp. &Scenedesmus sp. a-endosulfan Sethunathan et al., (2004)
Selenastrum capricornutum PAHs + heavy metals Ke et al.,(2010)
Chlamydomonas reinhardtii Hg, Cd & Pb Tuzun et al.,(2005)
Chlamydomonas reinhardtii Cu, Cd & Hg Bayramoglu et al., (2006)
Nannochloropsis oculata Pb Felisco and Billacura (2018)
Bleu-green Cyanophyta) Chemical pollutants References
Anaebaena doliolum Cd & Cu Sultan et al, (2007)
Anabaena sp. Cd Singh et al., (2012)
Anabaena flos aquae, Nostoc elepsosporum, Nostoc linkia & Anabaena variabilis BOD & COD Ghazal et al., (2018)
Oscillatoria brevis&Westiellopsis prolifica DO, BOD & COD Vijayakumar and Manoharan (2012)
Nostoc linckia Zn & Cd El-Enany and Issa (2000)
Nostoc muscorum Zn & Cu Goswami et al., (2015)
Microcystis sp. Cr, Cd & Cu Rai and Tripathi (2007)
Spirulina platensis, Streptomyces sp. &Arthrobacter sp. Cd, Cr, Ag & Au Gelagutashvili (2013)
Anabaena oryzae & Cyanosarcina fontana Fe, Cu, Pb & Mn Fawzya and Issa (2016)
Table 2.Macroalgae used for chemical pollutants removal.
Green (Chlorophyta) Chemical pollutants References
Cladophora fascicularis Cu Prabha et al., (2016)
Spirogyra Pb Prabha et al., (2016)
Spirogyra sp. Cr Gupta et al., (2001)
Spirogyra sp. Pb Gupta and Rostogi (2008a)
Spirogyra sp. Cu Gupta et al., (2006)
Spirogyra hyalina Cd, Hg, Pb, As & Co Ben Chekroun and Baghour (2008)
Codium vermilara & Spirogyra insignis Cd, Ni, Zn, Cu & Pb Romera et al., (2007)
Oedogonium sp. Pb Gupta and Rostogi (2008b)
Caulerpa racemosa Br Ben Chekroun and Baghour (2008)
Caulerpa racemosa Pb & Cd Dekhil et al, (2011)
Ulva lactuca Cu, Pb, Zn & Cd Saleh (2015)
Ulva lactuca Cd Saleh (2017b)
Ulva sp. Zn Badescu et al., (2017)
Ulva lactuca Cd Lupea,and Bulgariu |(2012)
Ulva lactuca Cd & Pb Sari and Tuzen (2008a)
Ulva lactuca Cu Murphy et al, (2007)
Ulva lactuca Cr Asnaoui et al., (2014)
Ulva sp., Enteromorpha sp. &Chaetomorpha sp. Fe, Al, Zn, Cd, Cu, As & Pb Gosavi et al., (2004)
Ulva fasciata As Christobe and Lipton (2015)
Ulva fasciata Cu Karthikeyan et al., (2007)
Brown (Phaeophyta) Chemical pollutants References
Durvillaea potatorum Cd Matheickal et al., (1999)
Padina sp. Cd Kaewsarn and Yu (2001)
Padina sp. Cu Prabha et al, (2016)
Padina pavonica Cd Saleh (2017b)
Sargassum sinicola Cd & Cu Prabha et al, (2016)
Sargassum sp. Cu Karthikeyan et al., (2007)
Sargassum fluitans Cu, Fe, Zn & Ni Ben Chekroun and Baghour (2008)
Sargassum natans &Sargassum vulgare Pb Ben Chekroun and Baghour (2008)
Sargassum wightii As Christobe and Lipton (2015)
Petalonia fascia Ni and Cu Schiewer and Wong (2000)
Laminaria hyperborea Zn, Ni & Cu Cechinel et al., (2016)
Laminaria hyperborea Zn Mazur et al., (2016)
Pilayella littoralis Cr, Fe, Al, Cd, Cu, Zn, Co & Ni Carrilho and Gilbert (2000)
Turbinaria conoides Pb Senthilkumar et al., (2007)
Fucus spiralis & Ascophyllum nodosum Cd, Ni, Zn, Cu & Pb Romera et al., (2007)
Ecklonia maxima Cu, Pb & Cd Feng et al., (2004)
Ascophyllum nodosum Au, Co, Ni & Pb Ben Chekroun and Baghour (2008)
Fucus vesiculosus Zn & Ni Ben Chekroun and Baghour (2008)
Fucus vesiculosus Zn, Cr & Fe Castro et al., (2017)
Fucus vesiculosus&Fucus spiralis Cu Murphy et al, (2007)
Ecklonia sp. Cr Yun et al., (2001)
Red (Rhodophyta) Chemical pollutants References
Acanthophora spicifera Cr, Pb, Cd & Hg Tamilselvan et al., (2011)
Ceramium virgatum Cd Sari and Tuzen (2008b)
Palmaria palmata Cu Murphy et al, (2007)
Palmaria palmata Pb, Cu, Ni, Cd & Zn Prasher et al., (2004)
Laurencia obtusa Cd, Co, Cr, Cu, & Ni Hamdy (2000)
Porphyra leucosticte Cd & Pb Ye et al., (2015)
Gracilaria fischeri Cu & Cd Chaisuksant (2003)
Gracilaria sp. Cd, Cu, Zn, Pb, & Ni Sheng et al., (2004)
Gracilaria corticata As Christobe and Lipton (2015)
Gracilaria sp. Cd & Cu Tonon et al., (2011)
Gellidium sp Cd Abd El Monsef et al, (2014)
Laurancia obtusa, Geldiella acerosa & Hypnea sp. Cu, Zn, Mn & Ni Ibrahim and Mutawie (2012)
Palmaria palmate&Polysiphonia lanosa Cd & Cu Baumann et al., (2009)
Palmaria decipiens &Georgiella confluens & Myrioqramme manqini As, Cd, Co, Cr, Cu, Fe, Mn, Mo, Ni, Pb, Se, Sr, V& Zn Farias et al., (2002)
Asparagopsis armata & Chondrus crispus Cd, Ni, Zn, Cu & Pb Romera et al., (2007)
CONCLUSION
From this point of view:
I. Algae could be considered as a friendly, economic, good and potent heavy metals biosorbent. Among algae, Overall Chlorella spp. in particularly C. Vulgaris microalga could be considered as the most effective algae species for heavy metals removal. Moreover, its richness in carbohydrate, protein, vitamins and minerals makes it commercially as health supplement or incorporated in food such as cereals. Due to the high importance of Chlorella spp. and its multiuse for many purposes; it is advice to its expanding culture worldwide.
II. For macroalgae, brown marine algae (Phaeophyta) among them have received much attention for heavy metals removal; and little studies
have been focused on the application of other algae phyla (Chlorophyta and Rhodophyta). Thereby, a expanding application of the latest algae phyla is requested.
III. Test various pretreatments that improve metal sorption capacity of algae, such chemical pretreatment by methanol/HCl are requested before employment it in pollutants removing. Leading finally to strong affinity of metals for carboxylic groups exist in the biomass surface, exhibiting a critical role in cations binding.
IV. Look for a new algae species that show remarkable heavy metal removal capacity and expansion their culture under laboratory or/and field conditions.
V. Expansion our knowledge on the application of a new algal species that show economic, efficient, and
practicable means for the heavy metals removal from industrial wastewater.
VI. Concentrated on brown algae among macrophyta due to their highly importance in heavy metals removal.
VII. Monitoring the new emerged pollutants especially those that toxicants, is requested.
However, after how long cycles the tested algae remain efficacy for elimination a given pollutants stay a question arise.
ACKNOWLEDGEMENT
I thank Professor Othman Ibrahim (Director General of AECS) and Professor MirAli Nizar (Head of Molecular Biology and Biotechnology Department) for their support.
REFERENCES
Abbas, S.H., Ismail, I.M., Mostafa, T.M., Sulaymon, A.H. (2014) Biosorption of heavy metals: A review. J Chem Sci Technol,3, 74-102. Abd El Monsef, W.S., Ragab A.A., Shalaby, E.A. (2014) Bioremediation of heavy metals by chemically-modifiedbiomass of algae and Eichhornia sp.Sky J Microbiol Res,2, 051 - 058. Ahluwalia, S.S., Goyal, D. (2003) Removal of lead from aqueous solution by different fungi. Ind J Microbiol ,43,237-241. Anayuri, R.A., Sari, A., Tuzen, M. (2009) Equilibrium thermodynamic and kinetic studies on biosorption of Pb(II) and Cd(II) from aqueous solution by macrofungus (Lactarius scrobiculatus) biomass. Chem Eng Journal,151, 255 - 261. Asnaoui, H., Khalis, M., Laaziri, A., Elbougarrani, O. (2014)Deconttamination of a solution of chromiumIV by marine algae (ulva-lactuca). Int J Innov Res in Adv Eng,1, 62-67. Badescu, I.S., Bulgariu, D., Bulgariu, L. (2017) Alternative utilization of algal biomass (Ulva sp.) loaded with Zn (II) ions for improving of soil quality. J Appl Phycol,29, 1069-1079. Balaji, S., Kalaivani, T., Rajasekaran, C., Shalini, M., Siva, R., Singh, R.K., Akthar, M.A. (2014)Arthrospira (Spirulina) species as
bioadsorbents for lead, chromium, and cadmium -a comparative study. Clean-Soil Air Water,42, 1790-1797.
Baumann, H.A., Morrison, L., Stengel, D.B. (2009) Metal accumulation and toxicity measured by PAM -Chlorophyll fluorescence in seven species of marine macroalgae. Ecotox Environ Safe,72, 10631075.
Bayramoglu, G., Tuzun, I., Celik, G.,Yilmaz, M., Arica, M.Y. (2006)Biosorption of mercury (II), cadmium (II) andlead (II) ions from aqueous system by microalgae Chlamydomonas reinhardtii immobilized in alginate beads.Int J Miner Process,81, 35-43.
Ben Chekroun, K., Baghour, M. (2008) The role of algae in phytoremediation of heavy metals: A review. J Mater Environ Sci, 4, 873-880.
Bilal, M., Rasheed, T., Ahmed, I., Iqbal, H.M.N. (2017) High-value compounds from microalgae with industrial exploitability—A review. Front Biosci (Sch. Ed.),9, 319-342.
Bilal, M., Rasheed, T., Sosa-Hernández, J.E., Raza, A., Nabeel F., Iqbal, H.M.N. (2018) Biosorption: An interplay between marine algae and potentially toxic elements—a review. Marine drugs,16, 65.
Bradl, H. (2002)Eeditor, Heavy metals in the environment: Origin, Interaction and Remediation Volume 6. London: Academic Press.
Bulgariu, L., Bulgariu, D. Rusu, C. (2015)Marine algae biomass for removal of heavy metal ions. Chapter from book Omega-3 Fatty Acids Produced from Microalgae, pp.611-648.
Carrilho, E.N., Gilbert, T.R. (2000) Assessing metal sorption on the marine alga Pilayella littoralis. J Environ Monit,2, 410-415.
Castro, L., Blázquez, M.L., González, F., Muñoz, J.A., Ballester, A. (2017) Biosorption of Zn(II) from industrial effluents using sugar beet pulp and F. vesiculosus: from laboratory tests to a pilot approach. Sci Total Environ,598, 856-866.
Cechinel, M.A.P., Mayer, D.A., Pozdniakova, T.A., Mazur, L.P., Boaventura, R.A.R., de Souza, A.A.U., de Souza, S.M.A.G.U., Vilar, V.J.P. (2016) Removal of metal ions from a petrochemical
wastewater using brown macro-algae as natural cation-exchangers. Chem Eng J,286, 1-15.
Chaisuksant, Y. (2003) Biosorption of cadmium (II) and copper (II) by pretreated biomass of marine alga Gracilaria fisheri. Environ Technol,24, 1501-1508.
Cheng, J., Yin, W., Chang, Z., Lundholm, N., Jiang, Z. (2017) Biosorption capacity and kinetics of cadmium (II) on live and dead Chlorella vulgaris. J Appl Phycol,29, 211-221.
Chong, A.M.Y., Wong, Y.S., Tam, N.F.Y. (2000)Performance of different microbial species in removing nickel and zinc from industrial wastewater. Chemosphere,41, 251-257.
Christobe, J., Lipton, A.P. (2015)Evaluation of macroalgal biomass for removal of heavy metal Arsenic (As) from aqueous solution. Int J Appl Innov Eng Manag,4, 94-104.
De Godos, I., Muñoz, R., Guieysse, B. (2012)Tetracycline removal during wastewater treatment in high-rate algal ponds. J Hazard Mater,229-230, 446-449.
Dekhil, A.B., Hannachi, Y., Ghorbel, A., Boubaker, T. (2011)Removal of lead and cadmium ions from aqueous solutions using dried marine green macroalga (Caulerpa racemosa). Int J Environ Res, 5, 725-732.
Delrue, F., Álvarez-Díaz, P.D., Fon-Sing, S., Fleury, G. Sassi, J-F. (2016)The environmental biorefinery: Using microalgae to remediate wastewater, a win-win paradigm. Energies,9, 132-150.
Dias, M.A. (2002) Removal of heavy metals by an Aspergillus terreus strain immobilized in polyurethane matrix. Lett Appl Microbiol,34, 46-50.
Djati Utomo, H., Tan, K.X.D., Choong, Z.Y.D., Yu, J.J., Ong, J.J., Lim, Z.B. (2016) Biosorption of heavy metal by algae biomass in surface water. J Environ Protect,7, 1547-1560.
El-Enany, A.E., Issa, A.A. (2000)Cyanobacteria as a biosorbent of heavy metals in sewage water. Environ Toxicol Pharma,8, 95-101.
FAO, (2014)The State of World Fisheries and Aquaculture. Food and Agriculture Organization of the United Nations, Rome.
Farias, S., Arisnabarreta, S.P., Vodopivez, C., Smichowski, P. (2002) Levels of essential and potentially toxic trace metals in Antarctic macro algae. Spectrochim Acta Part B,57, 2133-2140.
Fawzya, M.A., Issa, A.A. (2016)Bioremoval of heavy metals and nutrients from sewage plant by Anabaena oryzae andCyanosarcina fontana. Int J Phytoremed ,18,321-328.
Felisco, R.J.M., Billacura, M.P. (2018) Biosorption mechanism of microalgae Nannochloropsis oculata and the effect of Pb on its photosynthetic activity. Sci Int (Lahore), 30,115-119.
Feng, D., Aldrich, C. (2004)Adsorption of heavy metals by biomaterials derived from the marine alga Ecklonia maxima. Hydrometallurgy,73,1-10.
Gelagutashvili, E. (2013) Comparative study on heavy metals biosorptionby different types of bacteria. Open J of Metal,3, 62-67.
Ghazal, F.M., Mahdy, E-S.M., EL-Fattah, M.S.A., EL-Sadany, A.E.G.Y., Doha, N.M.E. (2018)The use of microalgae in bioremediation of the textile wastewater effluent. Nat and Sci,16, 98-104.
Goksungur, Y., Uren, S., Guvenc, U. (2005) Biosorption of cadmium and lead ions by ethanol treated waste baker's yeast biomass. Bioresour Technol, 96, 103-109.
Gosavi, K., Sammut, J., Gifford, S., Jankowski, J. (2004) Macroalgal biomonitors of trace metal contamination in acid sulfate soil aquaculture ponds. Sci Total Environ,324, 25-39.
Goswami, S., Diengdoh, O.L., Syiem, M.B., Pakshirajan, K., Kiran, M.G. (2015) Zn(II) and Cu(II) removal by Nostoc muscorum: a cyanobacterium isolated from a coal mining pit in Chiehruphi, Meghalaya, India.Canadian J Microbiol, 61, 209-215.
Gupta, V.K., Shrivastava, A.K., Neeraj, J. (2001) Biosorption of chromium(VI) from aqueous solutions by green algae Spirogyra species. Water Res, 35,4079-4085.
Gupta, V.K., Rastogi, A., Saini, V.K., Jain, N. (2006) Biosorption of copper(II) from aqueous solutions by Spirogyra species. J Colloid Interface Sci,296,59-63.
Gupta, V.K., Rostogi, A. (2008a) Biosorption of lead from aqueous solutions by green algae Spirogyra species: Kinetics and equilibrium studies. J Hazard Mater, 152,407-414.
Gupta, V.K., Rostogi, A. (2008b) Biosorption of lead(II) from aqueous solutions by non-living algal biomass Oedogonium sp. and Nostoc sp. - A comparative study. Coll Surf B,64, 170-178.
Gupta, M., Sarin, N.B. (2009) Heavy metal induced DNA changes in aquatic macrophytes: Random amplified polymorphic DNA analysis and identification ofsequence characterized amplified region marker. J Environ Sci,21, 686-690.
Hamdy, A.A. (2000) Biosorption of heavy metals by marine algae. Cur Microbiol,41, 232-238.
Hammouda, A., Gaber, A., Abdelraouf, N. (1995) Microalgae and wastewater treatment. Ecotox Environ Safe,31, 205-210.
Herrero, R., Cordero, B., Lodeiro, P., Rey-Castro, C., Vicente, M.E.S.D. (2006)Interactions of cadmium (II) and protons with dead biomass of marine algae Fucus sp. Marine Chem,99, 106-116.
Ibrahim, W.M., Mutawie, H.H.(2012)Bioremoval of heavy metals from industrial effluent by fixed-bed column of red macroalgae.Toxicol Indust Health,29, 38-42.
Iyer, A., Mody, K., Jha, B. (2005) Biosorption of heavy metals by a marine bacterium. Mar Pollut Bull, 50, 340-343.
Jamers, A., Blust, R., De-Coena, W., Griffinab, J.L., Jonesco, O.A.H. (2013)An omics based assessment of cadmium toxicity in the green alga Chlamydomonas reinhardtii. Aqua Toxicol, 126, 355- 364.
Javanbakht, V., Alavi S.A., Zilouei H. (2014)Mechanisms of heavy metal removal using microorganisms as biosorbent. Water Sci Technol,69, 1775-1787.
Jerold, M., Vigneshwaran, C., Surendhar, A., Prakash Kumar, B.G., Sivasubramanian,V. (2016)In book: Environmental Sustainability using Green Technologies, Chapter 5: Algal biosorption of heavy metals, Publisher: CRC publishers
Kaewsarn, P., Yu, Q. (2001) Cadmium (II) removal from aqueous solutions by pre-treated biomass of
marine alga Padina sp. Environ Pollut,112, 209213.
Karthikeyan, S., Balasubramanian, R., Iyer, C.S.P. (2007) Evaluation of the marine algae Ulva fasciata and Sargassumsp. for the biosorption of Cu (II) from aqueous solutions. Bioresour Technol,98, 452-455.
Ke, L., Luo, L., Wang, P., Luan, T., Tam, N.F.-Y. (2010)Effects of metals on biosorption and biodegradation of mixed polycyclic aromatic hydrocarbons by a freshwater green alga Selenastrum capricornutum. Bioresour Technol,101, 6950-6961.
Kshirsagar, A.D. (2013) Bioremedition of wastewater by using microalgae: Experiment study. Int J Life Sci Biotechnol Pharma Res, 2, 339-346.
Kumari, S.B., Kirubavathy, A.K., Thirumalnesan, R. (2006)Stability and water quality criteria of open drainage municipal sewage water at Coimbatore used for irrigation.J Environ Biol,27, 709-712.
Kumar, K.S., Dahms, H.-U., Won, E.-J., Lee, J.-S., Shin, K.-H. (2015)Microalgae—A promising tool for heavy metal remediation. Ecotoxicol Environ Safe, 113, 329-352.
Lawton, R.J., Mata, L., de Nys, R., Paul, N.A. (2013) Algal bioremediation of waste waters from land-based aquaculture using Ulva: Selecting target species and strains. PLoS ONE, 8, e77344.
Lima, S.A.C., Raposo, M.F.J., Castro, P.M.L., Morais, R.M. (2004)Biodegradation of p-chlorophenol by a microalgae consortium. Wat Res,38, 97-102.
Lupea, M., Bulgariu, L., Macoveanu, M. (2012) Biosorption of Cd(II) from aqueous solution on marine green algae biomass. Environ Eng Manag J,11, 607-615.
Mallick, N., Rai, L.C. (1992) Removal and assessment of toxicity of Anabena doliolum and Chlorella vulgaris using free and immobilized cells. World J Microbiol Biotechnol,8, 110 - 114.
Mandotra, S.K., Kumar, P., Suseela, M.R., Ramteke, P.W. (2014) Fresh water green microalga Scenedesmus abundans: A potential feedstock for high quality biodiesel production. Biores
Technol,156, 42-47.
Matheickal, J.T., Yu, Q., Woodburn, G.M. (1999) Biosorption of cadmium (II) from aqueous solutions by pre-treatedbiomass of marine alga Durvillaea potatorum. Water Res,33, 335-342.
Mazur, L.P., Pozdniakova, T.A., Mayer, D.A., Boaventura, R.A.R., Vilar, V.J.P., (2016) Design of a fixed-bed ion-exchange process for the treatment of rinse waters generated in the galvanization process using Laminaria hyperboreaas natural cation exchanger. Water Res,90, 354-368.
Mazur, L.P., Cechinel, M.A.P., de Souza, S.M.A.G.U., Boaventura, R.A.R., Vilar, V.J.P. (2018) Brown marine macroalgae as natural cation exchangers for toxic metal removal from industrial wastewaters: A review. J Environ Manag,223, 215-253.
McHugh, D.J. (2003) A Guide to the Seaweed Industry. Food and Agriculture Organization of the United Nations, Rome.
Mehta, S.K., Gaur, J.P. (2001)Removal of Ni and Cu from single and binary metal solutions by free and immobilized Chlorella vulgaris. Europ J Protistol,37, 261-271.
Mirghaffari, N., Moeini, E., Farhadian, O. (2015) Biosorption of Cd and Pb ions from aqueous solutions by biomass of the green microalga, Scenedesmus quadricauda. J Appl Phycol,27, 311320.
Murphy, V., Hughes, H., McLoughlin, P. (2007) Cu(II) binding by dried biomass of red, green and brown macroalgae. Water Res,41,731-740.
Nazal M.K. (2019) Chapter: Marine algae bioadsorbents for adsorptive removal of heavy metals; pp. 1-14.
Nielsen, M.M., Bruhn, A., Rasmussen, M.B., Olesen, B., Larsen, M.M., Moller, H.B., (2012)Cultivation of Ulva lactuca with manure for simultaneous bioremediation and biomass production. J Appl Phycol, 24, 449-458.
Ofer, R., Yerachmiel, A., Shmuel, Y. (2003) Marine macroalgae as biosorbents for cadmiun and nickel in water. Water Environ Res,75, 246-253.
Oswald, W.J., Gotaas, H.B. (1957) Photosynthesis in sewage treatment. Trans Am Soc Civ Eng,122, 73-
105.
Papazi, A., Kotzabasis, K. (2013)Rational management of dichlorophenols biodegradation by the microalga Scenedesmus obliquus. PLoS ONE,8.
Peng, F.-Q., Ying, G.-G., Yang, B., Liu, S., Lai, H.-J., Liu, Y.-S., Chen, Z.-F., Zhou, G.-J. (2014)Biotransformation of progesterone and norgestrel by two freshwater microalgae (Scenedesmus obliquus and Chlorella pyrenoidosa): Transformation kinetics and products identification. Chemosphere,95, 581-588.
Pinto, A.P., Mota, A.M., De Varennes, A., Pinto, F.C. (2004) Influence of organic matter on the uptake of cadmium, zinc, copper and iron by sorghum plants. Sci Total Environ,326,239-274.
Prabha, Y., Soni, S.K., Gupta, S. and Sonal. (2016) Potential of algae in bioremediation of wastewater: Current research. Int J Cur Microbiol Appl Sci,5, 693-700.
Prasher, S.O., Beaugeard, M., Hawari, J., Bera, P., Patel, R.M., Kim, S.H. (2004)Biosorption of heavy metals by red algae (Palmaria palmata). J EnvironTechnol,25, 1097-1106.
Rai P.K., Tripathi, B.D. (2007)Removal of heavy metals by the nuisance cyanobacteria Microcystis in continuous cultures: an eco-sustainable technology.Environ Sci,4, 53-59.
Rajfur, M. (2013)Algae-heavy metals biosorbent. Ecol Chem Eng, 20, 23-40.
Robertson-Andersson, D.V., Potgieter, M., Hansen, J., Bolton, J., Troell, M., Anderson, R., Halling, C., Probyn, T. (2008) Integrated seaweed cultivation on an abalone farm in South Africa. J Appl Phycol, 20, 579-595.
Romera, F., Gonzalez, A., Ballester, M.L., Munoz B.J.A. (2007) Comparative study of biosorption of heavy metals using differenttypes of algae. Biores Technol,98, 3344-3353.
Ryther, J.H., Tenore, K.R., Dunstan, W.M., Huguenin, J.E. (1972)Controlled eutrophication-increasingfood production from sea by recycling human wastes. Bioscience,22, 144.
Saleh, B. (2015) Physiological response of the green
algae Ulva lactuca (Chlorophyta) to heavy metals stress. J Stress Physiol Biochem, 11, 38-51.
Saleh, B. (2017a) Analytical methods employment for heavy metals pollution investigation in Ulva lactuca (Chlorophyceae) seaweed. J Bio Innov, 6, 624-633.
Saleh, B. (2017b)Cadmium biosorption investigation from aqueous solutions with Ulva lactuca (Chlorophyta) and Padina pavonica (Phaeophyta) seaweeds. J Stress Physiol Biochem, 13, 81-87.
Saleh, B., Al-Mariri,A. (2017)Antimicrobial activity of the marine algal extracts against selected pathogens. J Agri Sci Technol,19, 1067-1077.
Salgueiro, J. L., Pérez, L., Maceiras, R., Sánchez, A., Cancela, A. (2016) Bioremediation of wastewater using Chlorella vulgaris microalgae: Phosphorus and organic matter.Int J Environ Res, 10, 465-470.
Sari, A., Tuzen, M. (2008a) Biosorption of Pb (II) and Cd (II) from aqueous solution using green alga (Ulva lactuca) biomass. J Hazard Mater,152, 302-308.
Sari, A., Tuzen, M. (2008b) Biosorption of cadmium (II) from aqueous solution by red algae (Ceramium virgatum): Equilibrium, kinetic and thermodynamic studies. J Hazard Mater,157, 448-454.
Schiewer, S., Wong, M.H. (2000) Ionic strength effects in biosorption of metals by marine algae. Chemosphere,41, 271-282.
Senthilkumar, R., Vijayaraghavan, K., Thilakavathi, M., Iyer, P.V.R., Velan, M. (2007)Application of seaweeds for the removal of lead from aqueous solution. Biochem Eng J,33, 211-216.
Sethunathan, N., Megharaj, M., Chen, Z.L., Williams, B.D., Lewis, G., Naidu, R. (2004)Algal degradation of a known endocrine disrupting insecticide, a-Endosulfan, and its metabolite, endosulfan sulfate, in liquid medium and soil. J Agric Food Chem,52, 3030-3035.
Sharma, N.K., Rai, A.K. (2011) Biodiversity and biogeography of microalgae: Progress and pitfalls. Environ Rev,19, 1-15.
Sheng, P.X., Ting, Y.P., Chen, J.P., Hong, L. (2004) Sorption of lead, copper, cadmium, zinc, and nickel by marine algal biomass: Characterization of biosorptive capacity and investigation of
mechanisms.J Colloid Interface Sci, 275, 131-141.
Shilpi, G., Shilpi, S., Sunita, S. (2015) Tolerance against heavy metal toxicity in cyanobacteria: Role of antioxidant defense system. Int J Pharma Pharma Sci, 7, 9-16.
Singh, L.L., Chu, W.L., Phang, S.M. (2010) Use of Chlorella vulgaris for bioremediation of textile wastewater. Bioresour Technol,101, 7314-7322.
Singh, P.K., Rai, S., Pandey, S., Agrawal, C., Shrivastava, A.K., Kumar, S., Rai, L.C. (2012) Cadmium and UV-B induced changes in proteome and some biochemical attributes of Anabaena sp. PCC7120. Phykos, 42, 39-50.
Sode, S., Bruhn, A., Balsby, T.J.S., Larsen, M.M., Gotfredsen, A., Rasmussen, M.B. (2013) Bioremediation of reject water from anaerobically digested waste water sludge with macroalgae (Ulva lactuca, Chlorophyta). Biores Technol,14, 426-435.
Sultan, P., Williams, S.M.I, Arif, J.P., Ahamad, N. (2007)Biochemical basis of heavy metal induced stress tolerance in the N2 fixing Cyanobacterium Anabaena doliolum. Afr J Cln Exper Microbiol,8,8-22.
Tamilselvan, N., Saurav, K., Kannabiran, K. (2011)Biosorption of selected toxic heavy metals using algal species Acanthophora spicifera. Pharmacologyonline, 1, 518-528.
Tonon, A.P., Oliveira, M.C., Soriano, E.M., Colepicolo, P. (2011) Absorption of metals and characterization of chemical elements present in three species of Gracilaria (Gracilariaceae) Greville: a genus of economical. Rev Bras Farmacogn,21, 355-360.
Tüzün, I., Bayramoglu, G., Yalgin, E., Ba§aran, G., Qel, G., Arica, M.Y. (2005) Equilibrium and kinetic studies on biosorption of Hg(II), Cd(II) and Pb(II) ions onto microalgae Chlamydomonas reinhardtii. J Environ Manage,77,85-92.
Vijayakumar, S., Manoharan, C. (2012) Treatment of dye industry effluent using free and immobilized cyanobacteria. Bioremed Biodeg,3,2 - 6.
Volesky, B. (2003) Biosorption process simulation tools. Hydrometallurgy, 71, 179-190.
Wajahatullah, K., Rayirath, U.P., Subramanian, S.,
Jithesh, M.N., Prasanth, R., Mark, H.D., Alan, C.T., James, C.S., Jeff, N., Balakrishan, P. (2009) Seaweed extracts as biostimulants of plant growth and development. J Plant Growth Regul,28,386-399.
Wang, L., Min, M., Li Y., Chen, P., Chen, Y., Liu, Y., Wang, Y., Ruan R. (2010)Cultivation of green algae Chlorella sp. in different wastewaters from municipal wastewater treatment plant. Appl Biochem Biotechnol, 162, 1174-1186.
Wang, S., Wang, X., Poon, K., Wang, Y., Li, S., Liu, H., Lin, S., Cai, Z. (2013)Removal and reductive dechlorination of triclosan by Chlorella pyrenoidosa. Chemosphere,92, 1498-1505.
World, H. (1992) Organization, Environmental Health
Criteria 134: Cadmium. WHO, Geneva, Switzerland.
Ye,J., Xiao, H., Xiao, B., Xu, W., Gao, L., Lin, G. (2015)Bioremediation of heavy metal contaminated aqueous solution by using red algae Porphyra leucosticta. Water Sci Technol,72, 1662-1666.
Yun, Y.S., Parck, D., Park, J.M., Volesky, B. (2001)Biosorption of trivalent chromium on the brown seaweed biomass. Environ Sci Technol, 35, 4353-4358.
Zutshi, S., Bano, F., Ningthoujam, M., Habib, K., Fatma, T. (2014)Metabolic adaptations to arsenic-induced oxidative stress in Hapalosiphon fontinalis-339. Int J Inn Res Sci Eng Technol,3,9386-9394.
