Remediation of Heavy Metal-Contaminated Soils and ... - Springer Link

Chapter 19

Remediation of Heavy Metal-Contaminated Soils and Enhancement of Their Fertility with Actinorhizal Plants Nathalie Diagne, Mariama Ngom, Pape Ibrahima Djighaly, Daouda Ngom, Babou Ndour, Maimouna Cissokho, Mathieu Ndigue Faye, Alioune Sarr, Mame Oure`ye SY, Laurent Laplaze, and Antony Champion

19.1

Introduction

Land degradation is becoming a huge issue for agriculture development. This degradation is accelerated by environmental stresses that adversely affect ecosystem biodiversity and productivity. Among them, heavy metals are the most alarming and the most toxic inorganic substances which have contaminated a large area of land (Upadhyaya et al. 2010). Heavy metal pollution can be defined as an undesirable change in the physical, chemical, or biological characteristics of land and water that may or will harmfully affect animals and plants (Odum 1971). The commonly heavy metal found at contaminated sites are arsenic (As), cadmium N. Diagne (*) Centre National de Recherches Agronomiques (CNRA/ISRA), Bambey, Seńe´gal Laboratoire Commun de Microbiologie (IRD/UCAD/ISRA), Bel-Air, Dakar, Seńe´gal Laboratoire mixte international Adaptation des Plantes et microorganismes associe´s aux Stress Environnementaux (LAPSE), Centre de Recherche de Bel Air, Dakar, Seńe´gal e-mail: [email protected] M. Ngom Laboratoire Commun de Microbiologie (IRD/UCAD/ISRA), Bel-Air, Dakar, Seńe´gal Laboratoire mixte international Adaptation des Plantes et microorganismes associe´s aux Stress Environnementaux (LAPSE), Centre de Recherche de Bel Air, Dakar, Seńe´gal Laboratoire Campus de Biotechnologies Ve´ge´tales (LCBV), Dakar, Seńe´gal De´partement de Biologie Ve´ge´tale, Universite´ Cheikh Anta Diop de Dakar, Dakar, Seńe´gal P.I. Djighaly Laboratoire Commun de Microbiologie (IRD/UCAD/ISRA), Bel-Air, Dakar, Seńe´gal Laboratoire mixte international Adaptation des Plantes et microorganismes associe´s aux Stress Environnementaux (LAPSE), Centre de Recherche de Bel Air, Dakar, Seńe´gal De´partement d’Agroforesterie, Universite´ Assane Seck de Ziguinchor, Ziguinchor, Seńe´gal © Springer International Publishing Switzerland 2015 I. Sherameti, A. Varma (eds.), Heavy Metal Contamination of Soils, Soil Biology 44, DOI 10.1007/978-3-319-14526-6_19

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(Cd), copper (Cu), chromium (Cr), lead (Pb), mercury (Hg), nickel (Ni), and zinc (Zn) (GWRTAC 1997; Tahar and Keltoum 2011; Wang and Bjo¨rn 2014). Some of them like Cu, Fe, Mn, Zn, and Ni are necessary to plant and animal life, while others like Cd, Cr, and Pb are nonessential and/or toxic (Punz and Sieghardt 1993). Increasing contamination of heavy metal in soils has several sources such as the rapid urbanization due to the growing population, industrialization, intensive agriculture, and animal manures (Upadhyaya et al. 2010; Nacke et al. 2013). Besides the deterioration of environmental quality, heavy metals are hazardous to humans and animals and affect agricultural productivity of crops (Grataõ et al. 2005; Singh et al. 2011; Espıńa et al. 2014). It has been demonstrated that heavy metal-induced oxidative stress in plants disturbs the balance between oxidants and antioxidants in the cells (Upadhyaya et al. 2010; Juknys et al. 2012). These pollutants can be transferred to the food chain from the soil and affect human health (An et al. 2011). Heavy metals in soils are difficult to remediate, and without treatment the pollutants cannot be degraded. These environmental pollutants can remain in soil for long periods. Many physicochemical and biological strategies are used for the restoration of lands contaminated by pollutants (Wuana and Okieimen 2011). However, phytoremediation remains one of the most “eco-friendly,” sustainable, and low-cost method (Raskin et al. 1997). Phytoremediation can be defined as an in situ D. Ngom De´partement d’Agroforesterie, Universite´ Assane Seck de Ziguinchor, Ziguinchor, Seńe´gal B. Ndour • A. Sarr Centre National de Recherches Agronomiques (CNRA/ISRA), Bambey, Seńe´gal M. Cissokho • M.N. Faye Laboratoire Commun de Microbiologie (IRD/UCAD/ISRA), Bel-Air, Dakar, Seńe´gal Laboratoire mixte international Adaptation des Plantes et microorganismes associe´s aux Stress Environnementaux (LAPSE), Centre de Recherche de Bel Air, Dakar, Seńe´gal M.O. SY Laboratoire mixte international Adaptation des Plantes et microorganismes associe´s aux Stress Environnementaux (LAPSE), Centre de Recherche de Bel Air, Dakar, Seńe´gal Laboratoire Campus de Biotechnologies Ve´ge´tales (LCBV), Dakar, Seńe´gal De´partement de Biologie Ve´ge´tale, Universite´ Cheikh Anta Diop de Dakar, Dakar, Seńe´gal L. Laplaze Laboratoire mixte international Adaptation des Plantes et microorganismes associe´s aux Stress Environnementaux (LAPSE), Centre de Recherche de Bel Air, Dakar, Seńe´gal Equipe Rhizogene`se, UMR DIADE, IRD, 911 avenue Agropolis, 34394, Montpellier Cedex 5, France A. Champion Laboratoire Commun de Microbiologie (IRD/UCAD/ISRA), Bel-Air, Dakar, Seńe´gal Laboratoire mixte international Adaptation des Plantes et microorganismes associe´s aux Stress Environnementaux (LAPSE), Centre de Recherche de Bel Air, Dakar, Seńe´gal Equipe Rhizogene`se, UMR DIADE, IRD, 911 avenue Agropolis, 34394, Montpellier Cedex 5, France

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remediation strategy that uses vegetation and associated microbiota, soil amendments, and agronomic techniques to remove and contain environmental contaminants or render them harmless (Cunningham and Ow 1996; Helmisaari et al. 2007). Many species are used in phytoremediation to clean up toxic metal-contaminated sites (Fig. 19.1) (Kumar et al. 1995; Raskin et al. 1997). Among them, the actinorhizal plants which are nitrogen-fixing trees composed by eight families Betulaceae, Casuarinaceae, Coriariaceae, Datiscaceae, Elaeagnaceae, Myricaceae, Rhamnaceae, and Rosaceae are used in phytoremediation (Wall 2000). Plants of Casuarinaceae and Betulaceae families are the most widely planted around the world for the rehabilitation of degraded lands (Schwencke and Caru 2001; Diagne et al. 2013a, b). These plants are pioneer species well adapted to disturbed soils and abiotic stresses such as heavy metal (Sayed 2011; Lakhdari and Benabdeli 2012). They are able to be associated with different symbiotic soil microorganisms such as symbiotic mycorrhizal fungi and the nitrogen-fixing bacteria Frankia (Fig. 19.2)

Fig. 19.1 C. equisetifolia plantation in magnesite-mined outlands, India (It’s Karthikeyan who took the photo)

Fig. 19.2 (a) C. equisetifolia mycorrhizal roots; (b) actinorhizal nodule

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that mitigate the adverse effect of heavy metal and improve plant performance in stressed environments (Sayed 2011; Parao 2012). In this study, we will discuss (1) the use of actinorhizal plants in phytoremediation to clean up toxic metal, (2) the impact of mycorrhizal fungi and/or the nitrogen-fixing bacteria on plant adaptation and performance in heavy metal-contaminated sites, and (3) the impact of actinorhizal plantations on soil fertility and plant productivity.

19.2

Remediation of Heavy Metal-Contaminated Soils with Actinorhizal Plants

Experimentations using actinorhizal trees and particularly plants of Casuarinaceae and Betulaceae families were conducted worldwide for the remediation of soils contaminated by heavy metal (Rosselli et al. 2003; Mertens et al. 2004; Lee et al. 2009; Sayed 2011) (Fig. 19.1). However, plants’ responses to heavy metal vary considerably, and some species such as Casuarina equisetifolia and Alnus maritima tolerate high concentrations of heavy metal (Parao 2012). It has been reported that C. equisetifolia can tolerate 19 μg/g of Cr, 663 μg/g of Fe, and 13 μg/g of Ni (Claveria 2012). Some experiments in high level of fuel have also showed that C. equisetifolia can tolerate up to 10 g/kg of fuel in soil (Sun et al. 2004). Studies carried out by Lakharadi and Benabdeli (2012) in Mascara in Algeria have showed that C. equisetifolia can be successfully applied in biomonitoring of air pollution and heavy metal soil remediation (Dıáz-Martıńez et al. 2013). These authors have found a higher heavy metal concentration in C. equisetifolia needles collected in sites with a high traffic density and frequency of car stoppage. These chemical analyses revealed the presence of Pb, Zn, Cu, and Ni in C. equisetifolia needles. In addition, studies carried out by Parao (2012) showed that Alnus plays a major role in Fe and Mn remediation in soil. Samples from Alnus showed that the concentration of Fe varies from 3,982.12 ppm for the plantation of 8 months old to 93.33 ppm for Alnus trees years after plantation. For Mn, the concentration varies from 1,065.56 ppm after 8 months to 756.50 ppm 3 years after plantation. High concentrations of Cu have been also reported in Betula plants (Maurice and Lagerkvist 2000). Other ions like Zn are found accumulated at higher level in Alnus glutinosa leaves (Pulford et al. 2001). Black alders or Alnus glutinosa (L.) Gaertn grows naturally in the Taruskos forestry in Paneve˙zˇys region where 600 t of industrial sewage sludge was spread on the soil and accumulates some ions such as Ni, Cu, Pb, Zn, and Mn (Butkus and Baltrenaite 2007). These authors showed that Alnus glutinosa tolerates the presence of Zn up to 214 mg/kg. Compared to the black alder control, alders grown on sludge have accumulated about two times a large amount of Zn in leave (Butkus and Baltrenaite 2007). In naturally regenerated site in Yunnan province (Southwestern China), Nepalese alder (Alnus nepalensis) showed a great role in phytostabilization of Zn and Pb and phytoextraction of Cd (Jing et al. 2014).

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A pilot experiment to reclaim dredging area with A. firma and A. hursita has shown after 4 years of plantation that Alnus plant took metals up from the soil in the following order: Pb greater than Zn greater than Cu greater than Cr greater than As greater than Cd (Lee et al. 2009). However, these results have shown that A. firma is more tolerant to these pollutants than A. hursita. Regarding the plant density, their authors found that low plant density resulted in higher heavy metal uptake per plant, but the total heavy metal concentration was not different for plants planted at low and high density, suggesting that the plant density effect might not be important with regard to total uptake by plants.

19.3

Impact of Mycorrhizal Fungi or the Nitrogen-Fixing Bacteria on Actinorhizal Plant Adaptation and Performance in Heavy Metal-Contaminated Sites

19.3.1 Impact of Frankia on Actinorhizal Plant Adaptation and Performance in Heavy Metal-Contaminated Sites Species belonging to the Casuarinaceae family are able to form nitrogen-fixing symbioses with soil filamentous actinobacteria called Frankia (Wall 2000). They are collectively termed actinorhizal plants, and about 194 species and 24 genera have been identified (Benson and Silvester 1993). These symbiotic associations occur on the roots of host plant, and they lead to the formation of new root organs called actinorhizal root nodules (Fig. 19.2) where the bacteria are hosted and fix atmospheric nitrogen (Duhoux et al. 1996). Frankia formed extensive hyphae and multilocular sporangia (Fig. 19.3) located either terminally or in an intercalary position on the septate hyphae (Newcomb et al. 1979). Therefore, they provide to the host plant an unlimited source of nitrogen for its nutrition (Perrine-Walker

Fig. 19.3 Structures of the nitrogen-fixing actinobacteria Frankia. H hyphae, V vesicle, and S sporangia

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et al. 2011), and in exchange, they benefit from plant carbon sources (Pawlowski and Demchenko 2012). Resistance of Frankia strains and their impact on actinorhizal plant performance in heavy metal-contaminated soil are well documented. For instance, the sensitivity of 12 Frankia strains to heavy metals was determined by addition to the growth media at several concentrations of different metal ions including Cu2+, Pb2+, AgNO3, Na2HAsO4, NaAsO2, CdCl2, CoCl2, K2CrO4, CuCl2, and NiCl2 (Richards et al. 2002). Results showed that most of the Frankia strains were resistant to elevated levels of several heavy metals as AsO43 , Pb2+, SeO22 , Cu2 , and CrO42 . This study suggested that the mechanism of SeO22 resistance for Frankia strains seems to involve the reduction of the selenite oxyanion to insoluble elemental selenium which is much less toxic than selenite, whereas Pb2 resistance and Cu2 resistance may involve sequestration or binding mechanisms (Richards et al. 2002). Wheeler et al. (2001) showed that the yield of three Frankia strains was not affected significantly by 2.25 mM of nickel when cultured in vitro in the presence of propionate as carbon source and hydrolyzed casein as nitrogen source. It has been described that nickel is required for nitrogen-fixing bacteria including Frankia (Sellstedt and Smith 1990). Nickel is required for the synthesis of the uptake hydrogenases which catalyze the oxidation of hydrogen liberated by nitrogenase during the reduction of dinitrogen (Klucas et al. 1983). Oliveira et al. (2005) found that inoculation of A. glutinosa plants with Frankia spp. significantly increased the dry weight biomass and leaf N content by 197 % compared with the uninoculated controls when cultivated in an alkaline anthropogenic sediment. In the poor nutriment bauxite mine soils, in India, inoculated seedlings of C. equisetifolia by some suitable beneficial microbes including Frankia showed 90–100 % survival over the control seedlings (uninoculated plants). Plants inoculated with Frankia had also a significant growth as well as nutrient uptake (N, P, K) higher than the control after 3 months and also 2 years after planting (Karthikeyan et al. 2009). Inoculation of Alder (Alnus cordata Loisel) with selected Frankia strains in mine spoil afforestation plots showed a remarkable positive effect on alder aboveground biomass after 1 year planting (Lumini et al. 1994).

19.3.2 Impact of Arbuscular and Ectomycorrhizal Fungi on Actinorhizal Plant Adaptation to Heavy Metal-Contaminated Sites A mycorrhiza is a symbiotic association between a fungus and the roots of vascular plants (Sadhana 2014). Several actinorhizal species like Casuarina and Alnus can also be colonized by both ectomycorrhizal (ECM) and arbuscular mycorrhizal (AMF) fungi (Gardner 1986). The mycorrhizal fungi act as extensions of the root system (Fig. 19.2) and improve host nutrition by their ability to take up nutrients and water more efficiently than roots alone (Roy et al. 2007; Smith and Read 2008).

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They improve plant nutrient uptake and profit from plant carbon source. In addition, mycorrhizal fungi enhance plant performance and resistance to abiotic stresses (Sadhana 2014). Plants in symbiosis with AMF and ECM have the potential to be used for enhancing phytoremediation of heavy metal in contaminated soil thanks to their ability to take up heavy metal from an enlarged soil volume (Upadhyaya et al. 2010; Malekzadeh et al. 2012). Some mycorrhizal fungi can grow in the presence of diverse environmental stresses including heavy metal. For example, the tolerance to heavy metal of five ECM strains was tested by adding to the medium several concentrations (0.1– 400 μg/mL) of Al, Cu, Zn, Fe, Ni, Cd, Cr, Pb, and Hg (Tam 1995). Results showed that all ECM strains were tolerant to high concentrations of Fe and Pb and sensitive to low concentrations of Ni, Cd, and Hg. However, only Pisolithus tinctorius and Scleroderma sp. exhibited greater metal tolerance at high concentrations of Cu, while Hymenogaster sp. exhibited a great tolerance at high concentration of Al (Tam 1995). Even if some metals are micronutrients necessary for plant and microorganism growth, such as Zn, Cu, Mn, Ni, and Co, high concentrations of these metals in soil are toxic to plant, bacteria, and fungi (Leyval et al. 1997). However, it has been reported that mycorrhizal fungi can considerably reduce the uptake of heavy metals into plant cells and therefore allow them to thrive on heavy metal-polluted sites (Hildebrandt et al. 2007). The protection provided by ECM is due to the mycelia affording a physical barrier or mantle and may include metabolic processes such as intracellular metal accumulation and the extracellular precipitation of metals by metabolites from exudates (Khan et al. 2000). In their study, Karthikeyan et al. (2009) found that inoculation of C. equisetifolia plants with Glomus aggregatum alone on bauxite mine spoils increases their growth both in nursery and field experiments. Inoculated seedlings showed also 90–95 % survival on bauxite mine spoils after 2 years compared to uninoculated plants (35 %). A significant increase of leaf biomass and N, P, and K content was equally showed. Inoculation of alders (A. cordata Loisel.) with spores of G. fasciculatum or G. mosseae showed a positive effect on plant biomass after 1 year of planting in mine spoil (Lumini et al. 1994).

19.3.3 Impact of Frankia/AMF and/or EMF on Actinorhizal Plant Adaptation and Performance in Heavy Metal-Contaminated Sites Thanks to their ability to form symbiosis with nitrogen-fixing bacteria, Frankia, ECM, and/or AMF, actinorhizal plants are pioneer species which are able to grow well in a range of climates and disturbed soils. It is known that plant growth is often limited by the amount of available water, nitrogen, and phosphore in soil especially in degraded areas. Nitrogen is the most abundant component in the atmosphere, but

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only some prokaryotes as Frankia are able to use this form of nitrogen. These symbiotic relationships with Frankia and mycorrhizal fungi increase actinorhizal plant nutrition and water absorption unlike nonsymbiotic plants. Several studies showed that dual inoculation with Frankia and mycorrhizal fungi enhances actinorhizal plant growth and fitness more than single inoculation. In bauxite mine spoils in India, inoculation of C. equisetifolia plants with both selected Frankia and AM fungi (G. aggregatum) increased significantly their growth 2 years after planting compared to single inoculation and uninoculated plants (Karthikeyan et al. 2009). The triple microbial inoculants (Frankia + AMF + phosphobacterium) showed significantly increased growth and biomass, nodule number, percentage of AMF fungal infection, and collar diameter than control and other treatments. N, P, and K contents were also higher in AMF + Frankia and AMF + Frankia + phosphobacterium-inoculated trees. A percentage of survival of 100 % was observed in trees inoculated with Frankia + AMF + phosphobacterium against more than 95 % for the combination Frankia + AMF, 90–95 % for the individual microbial inoculants, and 35 % for the controls. Similar results were observed by Lumini et al. (1994). In mine spoils, inoculation of alders by both Frankia/G. fasciculatum and Frankia/G. mosseae produced a high degree of nodulation and mycorrhizal infection. Plant aboveground biomass was significantly increased by inoculation with these combinations after 1 year of outplanting in mine spoils compared to single inoculation treatments and uninoculated plants. About 500 D2H (cm3) of the biomass for Frankia/G. mosseae-treated trees, more than 400 D2H (cm3) for Frankia/G. fasciculatum-treated trees against less than 100 D2H (cm3) for the controls and plants inoculated separately with each fungal (Lumini et al. 1994). Synergetic inoculation of A. glutinosa in a highly alkaline anthropogenic sediment by G. intraradices and Frankia spp. increased significantly the number of spores in dry soil, plant nodule number, and dry weight (Oliveira et al. 2005). The total leaf area, shoot height, root collar diameter, and total plant dry weight were significantly greater when compared to those inoculated with one symbiont or the uninoculated plants. There was a significant increase of 277 % in leaf N content, 240 % in leaf P content, and 129 % in leaf K content in plants inoculated with both symbionts simultaneously when compared to the uninoculated plant. The dual inoculation showed also an increase of 531 % in chlorophyll a + b content compared to the controls (Oliveira et al. 2005).

19.4

Actinorhizal Plants Improve Fertility of Heavy Metal-Contaminated Soil

As microorganisms are the key of organic matter decomposition, assessment of soil microbial community structure and function may be useful to study the effect of potential plant remediation on soil quality. It is well known that heavy metals decrease plant growth and ground cover and reduce soil biodiversity (Pal et al. 2010). Contamination with heavy metal can modify soil physicochemical

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properties, and it has been reported by Zloch et al. (2014) that the metabolic activity of endophytic populations was strongly influenced by soil physicochemical properties and was significantly lower at a more contaminated site. In site planted with C. equisetifolia, Pe´rez et al. (2012) have reported that phytoremediation with C. equisetifolia improves soil quality and fertility by increasing the total N and P content in soil. On bauxite mine spoil planted with C. equisetifolia Frost, Karthikeyan et al. (2009) have found that inoculation with Frankia, AMF, and/or PSB increases C. equisetifolia N and P content. Given that the soil collected from bauxite mine spoils is acidic and poor in major nutrients (Karthikeyan et al. 2009), planting C. equisetifolia tree inoculated with Frankia, AMF, and/or PSB will be very useful because this species has an important biomass widely used in composting, and an increasing of N and P in C. equisetifolia needle will improve soil fertility of the site. The positive role on the improvement of soil fertility with actinorhizal trees used in phytoremediation has been also observed with Alnus species. After 10 years of revegetation with A. nepalensis in a phosphate mine in Kunyang, Yunnan Province, SW China, the assessment of soil quality showed an improvement of N and K available in soil and a decrease of total P concentration. Their results showed that A. nepalensis cleans up heavy metal, improves nutrient content and stability of the soil, and promotes the growth of microorganisms as a bioindicator for soil health after contamination remediation (He et al. 2013).

19.5

Conclusion

To satisfy the high demand for food in Africa, some high-efficiency and low-cost options for heavy metal remediation in soil need to be promoting to make lands available for agricultural activities. Phytoremediation, is one of the best technologies for cleaning up contaminated environments. However, this practice needs to be optimized by better understanding the complex interactions between soil, contaminants, microbes, and plants which depend in pedo-climatic parameters. As the main source of toxic heavy metal comes from inappropriate and illegal human actions, the population should be more aware to limit environmental heavy metal spreading to reduce food chain contamination by these pollutants for their well-being.

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