Abstract
Phytoremediation is an emerging technology that uses plants and their associated microbes to clean up pollutants from the soil, water, and air. In recent years, heavy metal phytoremediation assisted by plant beneficial actinomycetes has been highly used for cleaning up metal-polluted soils since these bacteria play an essential role in plant growth, metal/nutrient acquisition, metal detoxification, and alleviation of biotic/abiotic stress in plants. Direct plant growth promotion by actinomycetes is based on hormonal stimulation and improved nutrient acquisition by plants. Similarly, diverse mechanisms, viz., soil acidification and production of metal mobilizing/immobilizing substances by actinomycetes, are involved in heavy metal uptake by plants, which is often directly connected with the efficiency of phytoremediation process. Based on these beneficial plant-actinomycetes interactions, it is possible to develop microbial inoculants as environmentally friendly bio-tool for use in heavy metal phytoremediation. In this study, we highlight the diversity and plant growth beneficial features of actinomycetes and discuss their potential role on plant growth and phytoremediation process in metal-polluted soils.
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Keywords
- Plant-associated microorganisms
- Actinomycetes
- Heavy metals
- Rhizosphere
- Siderophores
- 1-Aminocyclopropane-1-carboxylic acid
14.1 Introduction
The development of numerous technologies and industrialization ends up with the result of release of heavy metals as pollutants into the environment (Doble and Kumar 2005; Rajkumar et al. 2009). Particularly, the contamination of soil with heavy metals is a major worldwide problem in the current decade (Kamran et al. 2014). The heavy metal accumulation in soil adversely affects both the ecosystem and human health. Although some metals are essential for life, they are highly toxic to microorganisms (Fig. 14.1), plants, animals, and humans at higher concentrations. They affect various physiological and biochemical process by displacing other metal ions, blocking essential functional groups, disintegrating cell organelles (Vangronsveld and Clijsters 1994), acting as genotoxic substance, and disrupting the physiological process such as photosynthesis, respiration, protein synthesis, and carbohydrate metabolism.
Application of various physical, chemical, and biological strategies for decontaminating the polluted sites is a challenging task because heavy metals cannot be degraded and thus persist in the environment indefinitely. In order to clean up the contaminated sites, heavy metals should be concentrated and extracted from the contaminated sites by conventional methods for proper disposal or reuse. Although various strategies (such as land filling, excavation, fixation, solidification, and leaching) have been applied to remediate the contaminated sites, most of these methods are either extremely costly or simply involve the isolation of the contaminated sites or adversely affect the soil biological activity and fertility (Pulford and Watson 2003; Wu et al. 2010). Currently, the biological-based technique has been extensively used as an alternative method to remove pollutants from air, soil, and water or to render pollutants harmless (Chowdhury et al. 2015). “Phytoremediation” is one of the key processes of bioremediation that involves the use of plants and their associated microbes to relief, transfer, stabilize, or degrade the pollutants from soil, sediments, surface waters, and groundwater (Elekes 2014; Paz-Ferreiro et al. 2014; Laghlimi et al. 2015). The concept of phytoremediation was first proposed by Chaney (1983), which paved the way for the development of process of removing environmental contaminants using plants. The success of phytoremediation is dependent on the potential of the plants to tolerate the metal stress and produce high amount of biomass within a relatively short period. In recent years, plant-associated beneficial microbes have been used to enhance heavy metal phytoremediation process (Rajkumar et al. 2012). The plant-associated microbes accelerate phytoremediation process in metal-polluted soils by promoting plant growth and play a significant role in altering heavy metal accumulation in plants through producing various metabolites (e.g., siderophores, organic acids, and plant growth regulators) and various reactions in the rhizosphere (e.g., acidification, chelation, precipitation, and oxidation-reduction reactions). In turn, plant roots release nutrients through exudation which support the growth, survival, and colonization potential of microflora, involved in phytoremediation process.
Actinomycetes are gram positive, aerobic, sporulating, and filamentous bacteria which are ubiquitous in soils. Actinomycetes gain their importance among the researchers due to the production of enormous secondary metabolites and enzymes including antibiotics, degrading enzymes, enzyme inhibitors, immunosuppressants, phytotoxins, phytohormones, pesticides, and insecticides (Erikson 1949; Bèrdy 1995; Park et al. 2002; Hamaki et al. 2005; Imada 2005; Doumbou et al. 2011). They also directly promote plant growth by producing phytohormones (auxin, cytokinins, and gibberellins) and siderophore, solubilizing phosphate, fixing atmospheric nitrogen, and suppressing stress-ethylene production in plant through 1-amino cyclopropane-1-carboxylate (ACC) deaminase activity (Misk and Franco 2011; Sadeghi et al. 2012; Harikrishnan et al. 2014a) (Table 14.1). Moreover, the actinomycetes possess many properties that make them good candidates for application in bioremediation of soils contaminated with inorganic and/or organic pollutants. They produce extracellular enzymes that degrade a wide range of complex organic compounds. They play an important role in the recycling of organic carbon and are able to degrade complex polymers by production of extracellular degrading enzymes and peroxidases (Goodfellow and Williams 1983; Ball et al. 1989; Pasti et al.1990; Mason et al. 2001). Therefore, the utilization of metal-resistant actinomycetes, which are associated with plants, could be of particular importance as they can provide/solubilize nutrients such as Fe and P to plants, which could reduce the toxic effects of heavy metals. In addition, the metabolites produced by actinomycetes (e.g., siderophores and organic acids) bind Fe and other heavy metal ions and thus enhance their bioavailability in the rhizosphere of plants (Braud et al. 2009; Rajkumar et al. 2010). The resulting increase in plant growth and heavy metal accumulation by plants enhance the efficiency of phytoremediation in metal-contaminated soil.
This paper details recent advances in understanding plant and actinomycetes interaction and describes how their beneficial partnerships can be exploited as a strategy to accelerate plant growth and phytoremediation potential in heavy metal-polluted soils.
14.2 Actinomycetes and Heavy Metal Interaction
Microbial mechanisms conferring both plant growth promotion and heavy metal resistance have significant environmental importance because of their potential use in phytoremediation. In order to survive in metal-polluted environment, actinomycetes have evolved a number of mechanisms, by which they tolerate high concentrations of heavy metals (Pavel et al. 2013). Actinomycetes have been shown to alter heavy metal toxicity/bioavailability through various metal-independent mechanisms including (a) reduction of cellular sensitivity, (b) siderophore-heavy metal complexation, (c) intracellular metal sequestration, and (d) exclusion through permeability barriers. Several actinomycetes can adopt to resist the toxicity of heavy metals by altering the sensitivity of cellular components. Particularly, the mutations and DNA repair mechanisms may contribute to the protection toward plasmid and genomic DNA. Similarly, the metal-resistant components such as metallothioneins produced by actinomycetes can effectively bind heavy metals (Stillman 1995; Garbisu and Alkorta 2003) by which they can mobilize or immobilize and thus reduce their toxicity to tolerate heavy metal. For instance, glutathione offers resistance to the cell by suppressing the free radical formation from Cu(II) and Fe(II) and also to Ag(I), Cd(II), and Hg(II) (Rouch et al. 1995; Bruins et al. 2000). Similarly, the production of siderophores by actinomycetes can also play an important role in complexing toxic metals and in decreasing their toxicity. Siderophores are the iron-chelating secondary metabolites produced by various microorganisms under iron-limiting conditions. Actinomycetes are abundant producer of siderophores which plays a key role in the remediation of heavy metals. Many siderophores (e.g., desferrioxamine B, desferrioxamine E, rhodotorulic acid) are relatively stable biomolecules, protected from environmental peptidases and lytic enzymes by modifying structural composition (Sessitsch et al. 2013). In general, the siderophores produced by rhizosphere microbes form complexes with Fe(III) at the soil interface, desorb Fe from soil matrix, and thus increase Fe solubility and bioavailability in the soil solution. The siderophores also possess affinity to other trace element ion (Hider and Kong 2010) by which the bacteria reduce the harmful effects of metal and help in phytoremediation process. Dimkpa et al. (2009a, b, c) reported that the bacterial culture filtrates containing three hydroxamate siderophores secreted by Streptomyces tendae F4 significantly promoted plant growth and enhanced the uptake of Cd and Fe by cowpea relative to the control. Similarly, a recent study by Ji et al. (2012) observed that the production of siderophore desferrioxamine B (DFOB) accounted for the increased uptake of Fe and Pu by bacteria and reported that Pu4+-DFOB and Fe3+-DFOB complexes inhibit uptake of the other ions and compete for shared binding sites or uptake proteins. These results suggest that Pu-siderophore complexes can generally be recognized by Fe-siderophore uptake systems of microbes. Similarly, siderophores also played an important role in biocontrol of plant pathogens and in enhancement of plant growth promotion (Shanmugaiah et al. 2015).
The mechanism of metal tolerance exhibited by the actinomycetes is also due to the ability of its cell wall to bind with metal ions and accumulate in intracellular at higher concentrations (Lin et al. 2011; Singh et al. 2014; El Baz et al. 2015). For instance, a recent study by Lin et al. (2011) demonstrated the intracellular accumulation of Zn2+ and Cd2+ in a novel species, Streptomyces zinciresistens, under in vitro conditions and reported the interaction of heavy metals with amino, carboxyl, hydroxyl, and carbonyl groups accounted for the observed metal biosorption. In addition, certain actinomycetes reduce mobility of heavy metals through oxidation or reduction reactions. Such transformation especially plays a key role in the reduction of the toxicity of certain elements such as Cr and Hg in soils. For example, a Streptomyces sp. isolated from riverine sediments was shown to reduce the mobile and toxic CrO4 2− to non toxic Cr3+ (Amoroso et al. 2000). In a similar study, Ravel et al. (1998) demonstrated the Hg reducing potential of Streptomyces sp. isolated from the Baltimore Inner Harbor, at a site heavily contaminated with metal. They reported that this bacterium significantly reduced Hg(II) to elemental and volatile Hg and thereby reduce their toxicity to tolerate Hg.
Actinomycetes can also reduce the heavy metal bioavailability through producing extracellular polymeric substance (EPS). The EPSs are high-molecular-weight polymers which are composed of sugar residues. Lead, cadmium, and uranium are the most common heavy metals which bind to the EPS which results in the restriction of heavy metal entry in the cell. Albarracin et al. (2008) investigated biosorption potential of a copper-resistant Actinobacterium, Amycolatopsis sp. ABO, and found that these isolates were able to accumulate 25 mg/g of Cu. Intracellularly copper was distributed in cytosolic fraction (86 %), cell wall (11 %), and ribosome/membrane fraction (3 %).
The cells exposed to excess concentration of heavy metal has to manage with the production of toxic reactive oxygen species including superoxide anions in the Fenton reaction (Stohs and Bagchi 1995). These molecules are detoxified via superoxide dismutases (SODs) which dismutate the superoxide to O2 and H2O2 (Fridovich 1995). Subsequently, the hydrogen peroxide is detoxified in a catalase-mediated reaction. Schmidt et al. (2005) isolated a strain Streptomyces acidiscabies which showed tolerance to various metals (Ni, Cu, Cd, Cr, Mn, Zn, and Fe) conferred by Ni-containing SODs. The gene sodN code for the Ni-containing SODs is not only activated by Ni but also Cu, Fe, and Zn. Summers (1985) has reported that Hg-resistant Streptomyces sp. was able to detoxify the Hg through converting Hg2+ to volatile Hg0 by mercuric reductase enzyme.
The largest mechanism of metal-resistant system in microbes is active transport or efflux system. Some efflux systems involve ATPases, and others are chemiosmotic ion/proton pumps. These mechanisms actively pump back toxic ions that have entered the cell out of the cell via active transport (ATPase pump) or diffusion (chemiosmotic ion/proton pump). As, Cr, and Cd are the three metals most commonly associated with efflux resistance. It has been shown that a particular family of Actinobacteria including Streptomyces and Mycobacterium sp. use efflux-like mechanism for metal removal and antibiotic tolerance. An example is the ABC transport system for antibiotics, which can also be used as efflux pump for many metals (Borges-Walmsley et al. 2003). Albarracin et al. (2005) explained that the Cu resistance mechanisms of actinomycetes could be similar to that encountered in other bacteria such as the PcoABCDRS system of Escherichia coli or its homologue CopABCDRS of Pseudomonas sp. and Xanthomonas campestris (Nies 1999). Thus, the conservation of Cu pumps along evolution may indicate that uptake, reduction, or efflux of copper in actinomycetes could be also due to P-type ATPases. The schematic representation of metal-resistant mechanisms of actinomycetes in metal-polluted soil is presented in Fig. 14.2. Taken together, these reports clearly indicate the potential of actinomycetes to tolerate/reduce heavy metal toxicity and suggest that suitability of these microbes for heavy metal bioremediation.
14.3 Heavy Metal Phytoremediation
The emerging technology of bioremediation which paved the potential way for removal of heavy metals is phytoremediation. The term phytoremediation denotes the broaden area of remediation of polluted environment using plants which includes:
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1.
Phytoextraction: Cultivation of metal hyperaccumulating plants to remove the metals by concentrating them in harvestable parts of the plant
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2.
Rhizofiltration: Adsorption/precipitation of metals onto roots or absorption by roots of aquatic metal-tolerant plants
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3.
Phytostabilization: Immobilization of metals in the soils by adsorption onto roots or precipitation in the rhizosphere
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4.
Phytovolatilization: Conversion of pollutants to volatile form and their subsequent release to the atmosphere
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5.
Phytohydraulics: Absorption of large amount of water by fast-growing plants and prevent expansion of contaminants into adjacent uncontaminated areas
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6.
Rhizodegradation: Decomposition of organic pollutants by rhizosphere microorganisms
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7.
Phytoresaturation: Revegetation of barren area by fast-growing plants that cover soils and thus prevent the spreading of pollutants into environment (Masarovičová and Kráľová 2012)
Although a large number of plants are tolerating/accumulating high concentrations of heavy metals, the adverse environmental conditions particularly poor soil quality, higher concentrations of metals, multi-metal-contaminated soils, etc., generally impair the plant metabolism and thus reduce growth, survival, and overall phytoremediation potential in polluted soils. To overcome this limitation, the plant-associated bacteria have been extensively used as inoculants that confer plant metal tolerance, improve plant growth and health, mobilize/immobilize heavy metals, and are able to maintain a stable relationship with plants in metal-polluted soils. The following sections summarize the effects of plant-associated actinomycetes on plant growth in metal-polluted soils (Fig. 14.3).
14.4 Plant Growth-Promoting (PGP) Potential of Actinomycetes
Actinomycetes are recognized as a potential group of rhizobacteria which influence the plant growth, yield, and nutrient uptake by an array of mechanisms including the production of auxins, ACC deaminase, nitrogen fixation, siderophore production, and phosphate solubilization. Actinomycetes directly regulate plant physiology by mimicking synthesis of plant hormones, whereas other microorganisms increase mineral and nitrogen availability in the soil as a way to augment growth. The isolates could exhibit more than two or three PGP traits, which may promote plant growth directly, indirectly, or synergistically (Yasmin et al. 2007).
14.4.1 Indole-Acetic Acid (IAA)
Auxins are classified as the main phytohormone which regulate growth, ontogeny, morphogenesis, and adaptive and repair processes in plants (Shatheesh Kumar 2011). It was shown that auxins play an important role in root formation, elongation, promotion of ethylene production, and fruit ripening (Table 14.2). Among the numerous auxins that can be produced by plants and microorganisms, IAA, have received increasing attention as potential compounds to improve the plant growth and development. Experiments with Citrus reticulata revealed that the inoculation with the Nocardiopsis of actinomycetes increased the shoot height, shoot fresh weight, and root fresh weight from 20.2 % to 49.1 %, 14.9 % to 53.6 %, and 1.6 % to 102 %, respectively (Shutsrirung et al. 2013). This effect was attributed to the increased level of IAA (222.8 μg/mL) produced by the strain that was able to promote the plant growth. Harikrishnan et al. (2014a) assessed the ability of IAA producing Streptomyces aurantiogriseus to promote the growth of rice (Oryza sativa) plants and reported that S. aurantiogriseus, which produces high levels of IAA, increased the root and shoot length from 3.3 to 9 cm and 3.63 to 10.2 cm, respectively. Likewise, Cruz et al. (2015) also observed that the inoculation with IAA producing actinomycetes increased the growth and yield of rice under greenhouse conditions. The inoculation with Streptomyces sp. that had been isolated from wheat field has also been studied in detail (Sadeghi et al. 2012). These bacteria significantly reduced the toxicity of salt stress in wheat plants and promoted the plant growth and nutrient (N, P, Fe, and Mn) uptake under in vivo conditions. Here, it was suggested that IAA production together with other plant growth-promoting mechanisms, such as phosphate solubilization and siderophore production, accounted for the observed increase in growth of the test plants. Several of the plant-associated actinomycetes have also been reported to protect the plants from various soil-borne pathogens (Verma et al. 2011; Harikrishanan et al. 2014a, b). For instance, Verma et al. (2011) reported that the inoculation of spore suspension of Streptomyces strain AzR-051 significantly promoted plant growth and antagonized the growth of Alternaria alternata, causal agent of early blight disease in tomato plant.
14.4.2 Siderophore Production
Among the various plant growth-promoting traits, the production of siderophores by bacteria is of special significance because of its metal-chelating properties which play pivotal roles in increasing the Fe concentration in the rhizosphere soils and its uptake by plants. Valencia-Cantero et al. (2007) demonstrated the potential of siderophore-producing actinobacterial strain Arthrobacter maltophilia to protect Phaseolus vulgaris (common bean) form alkaline stress and reported this effect may be due to increased level of siderophores produced by the A. maltophilia that were able to increase Fe availability in the rhizosphere of the plants. Rungin et al. (2012) reported that the inoculation of an endophytic Streptomyces sp. GMKU 3100 to rice and mung bean plants significantly increased root and shoot biomass and length of test plants compared with non-inoculated and siderophore-deficient mutant treatments. This study indicates that siderophores of Streptomyces sp. GMKU played a major role in making sequestered iron available to the plant. Since the siderophores in rhizosphere soil may form complexes with other heavy metal ions and minimize the toxic effects of free metal ions, the heavy metal-siderophore complex is considered as less toxic than the free form of heavy metals. Dimkpa et al. (2008) have pointed out metal-chelating properties of siderophores, accounted for reduced heavy metal toxicity and increased auxin production in plants. They attributed the alleviation of metal toxicity to siderophore and metal complexation, thus protecting auxin from the toxic effects of free form of toxic metals.
14.4.3 ACC Deaminase Activity
Another important way in which the actinomycetes might influence the host plant growth is the utilization of ethylene precursor ACC as the sole source of nitrogen into α-ketobutyrate and ammonia. Actinomycetes containing ACC deaminase metabolize ACC, thereby lowering stress-ethylene level and enhancing plant growth (Glick 2005). Kibdelosporangium phytohabitans sp. KLBMP 1111T, a novel endophytic actinomycete isolated from root of the oilseed plant Jatropha curcas, has the ability to utilize ACC as a sole source of nitrogen via ACC deaminase enzyme. It also has the ability to produce siderophore and IAA (Xing et al. 2012). Halotolerant non-Streptomycete Actinobacteria such as Micrococcus yunnanensis, Corynebacterium variabile, and Arthrobacter nicotianae isolated from saline coastal region of Yellow river were reported to exhibit ACC deaminase activity and were able to significantly promote the growth of canola plants under salt stress condition (Siddikee et al. 2010). Similarly, El-Tarabily (2008) demonstrated that Streptomyces filipinensis no. 15 was able to reduce the level of ACC in roots and shoots promotes the growth of the tomato plants. They attributed this effect to the ability of actinomycetes to lower endogenous ACC level and low stress-ethylene accumulation.
14.4.4 Nitrogen Fixation
Nitrogen fixation is a process by which atmospheric nitrogen (N2) is converted into ammonia (NH3) (Wagner 2011), which can be assimilated by plants for the synthesis of nitrogenous biomolecules. A few species of Arthrobacter, Agromyces, Corynebacterium, Mycobacterium, Micromonospora, Propionibacteria, and Streptomyces have been shown to possess N2 fixation trait. Similarly free-living or symbiotic Frankia can also enhance plant growth and development in different soils and climate regions through nitrogen fixation. Particularly, the actinorhizal nitrogen fixation (symbiotic association between Frankia and dicotyledonous plants) plays a major role in establishing the plantations at adverse sites (Diagne et al. 2013). Similarly, some species of Thermomonosporaceae and Micromonosporaceae family also demonstrated to fix atmospheric nitrogen (Valdés et al. 2005). Similarly, Streptomyces thermoautotrophicus has been reported to utilize N2 as a sole nitrogen source when growing chemolithoautotrophically with CO or H2 and CO2 under aerobic conditions at 65 °C (Gadkari et al. 1992).
14.4.5 Phosphate Solubilization
Phosphorus is the second most important nutrient for plants, after nitrogen. It exists in soil as mineral salts or incorporated into organic compounds. Phosphate deficiency is one of the limiting factors in crop production. Microbes are able to solubilize insoluble phosphates in metallic complexes or in hydroxyapatite and release free phosphates (Rodríguez and Fraga 1999). Recent studies investigating the role of actinomycetes in plant growth promotion have demonstrated that the bacterial colonization often results in increased P solubilization and its uptake by plants. For instance, the increased plant growth and P uptake have been reported on the inoculation of Streptomyces griseus (Hamdali et al. 2008a, b), Streptomyces mhcr0816 and mhce0811 (Jog et al. 2012), Microbacterium sp. F10a (Sheng et al. 2009) in wheat plant, Streptomyces, and Thermobifida in Trifolium repens (Franco-Correa et al. 2010).
Although previous studies suggest that the inoculation of plants with beneficial actinomycetes could be a suitable approach for plant growth promotion, several authors have pointed out that single plant growth-promoting trait was not solely responsible for the plant growth. A large number of studies confirm the existence of cumulative effects of microbes such as the production of IAA, ACC deaminase activity, nitrogen fixation, siderophore production, and phosphate solubilization. For instance, Selvakumar et al. (2015) recently reported the potential of osmotolerant Actinobacterium Citricoccus zhacaiensis B–4 on the growth of onion plants under PEG-induced drought stress and reported that Actinobacterium improved the seedling vigor and germination rate of onion seeds (cv. Arka Kalyan) at osmotic potentials up to −0.8 MPa. They attributed this effect to the ability of the bacterium to exhibit various plant growth-promoting traits including the production of IAA and GA3, solubilization of phosphate and zinc, and ACC deaminase activity. Similarly, Mrinalini and Padmavathy (2014) also demonstrated that endophytic Streptomyces sp. Mrinalini7, isolated from neem plant, was able to promote the growth of tomato seedling through several plant growth-promoting traits such as IAA, ACC deaminase, phosphate solubilizing, siderophore, and ammonia production. These examples illustrate mechanisms, by which actinomycetes improve the plant growth and reflect the suitability of these microbes for improving heavy metal phytoremediation process.
14.5 Actinomycetes in Heavy Metal-Polluted Soils
Heavy metal contamination not only affects the plant growth and development but also influences the growth, survival, and activity of plant-associated microbes in polluted sites. However, numerous studies have demonstrated that actinomycetes isolated from metal-polluted soils exhibit multiple-metal tolerance as they have adopted to such environment and play an important role in metal detoxification process in the rhizosphere soil that determines the plant quality and yield (Ahemad and Kibret 2014). For instance, Gremion et al. (2003) characterized the metabolically active bacteria in heavy metal-contaminated rhizosphere soil of Thlaspi caerulescens using 16S ribosomal DNA and reverse-transcribed 16S rRNA clone libraries and reported that the dominant part of the metabolically active group of bacteria was Actinobacteria in both bulk and rhizosphere soil. Likewise, numerous studies have demonstrated the Actinobacteria as a consistently dominant group together with α Proteobacteria in metal-contaminated soils (Lazzaro et al. 2008; Karelova et al. 2011; Tipayno et al. 2012), which suggest a potential adaptation of the actinomycetes population to the heavy metal stress condition. The strains Streptomyces sp. A160 and S164 and Streptomyces fradiae A161 isolated from the soil of the Bay of Bengal showed the resistance to Cu up to 480 mg/L. Further, these strains also exhibited antibacterial and antifungal activity against wide range of pathogenic microbes. Moreover, the filamentous nature of the actinomycetes makes them as a potential heavy metal accumulator (Panday et al. 2004). Recently, Daboor et al. (2014) isolated heavy metal-resistant Streptomyces chromofuscus K101 from Nile River and assessed its heavy metal absorption potential. They found that S. chromofuscus was able to absorb high concentrations of metals with the order of Zn2+>Pb2+>Fe2+ in single or mixture metal reaction. Similarly, Hamedi et al. (2015) assessed cadmium accumulation potential of Promicromonospora sp. UTMC 2243 and found that the isolate was able to remove 96.5 % of Cr from aqueous solution. Vinod et al. (2014) reported Cr, Cu, Pb, and Zn accumulation potential of metal-resistant Streptomyces roseisederoticus (V5), Streptomyces flavochromogenes (V6), Streptomyces vastus (V7), and Streptomyces praguaeneses (V8) isolated from the rhizosphere soil of Casuarina equisetifolia. It was found that the S. roseisederoticus (V5) exhibited highest biosorption capacity for Cr, whereas S. flavochromogenes (V6) exhibited highest biosorption for Pb.
Several authors have pointed out that actinomycetes and their interactions with heavy metals (e.g., heavy metal biosorption/bioaccumulation, oxidation/reduction, and metal mobilization/immobilization) greatly influence the biomass production and quantity of metal accumulation in plants growing on metal-contaminated field soils. The following sections describe how the metal-resistant actinomycetes influence the plant growth and heavy metal uptake by plants in polluted soils (Table 14.3).
14.6 Role of Actinomycetes in Heavy Metal Phytoremediation
The functioning of plant and microbial interaction can be influenced by properties of rhizosphere soil. Actinomycetes play significant roles in plant growth under adverse environmental conditions by solubilizing plant nutrients, maintenance of soil structure, mobilization/immobilization of toxic chemicals, and controlling of plant pathogens (Giller et al. 1998; Elsgaard et al. 2001; Filip 2002; Jing et al. 2007). Besides, actinomycetes and their host plants can form specific associations in which the plant provides nutrients through root exudation that induces the growth, survival, and colonization potential of rhizosphere microbes. The metal-tolerant actinomycetes, such as Streptomyces, Amycolatopsis, and Rhodococcus (Trivedi et al. 2007; El Baz et al. 2015; Sunil et al. 2015), have been found to have potential to improve the plant growth and heavy metal mobilization or immobilization in metal-polluted soils. The abundant presence of actinomycetes in the metal-contaminated rhizosphere soil and its ability to withstand extreme environment make it suitable as a potential microbe which assisted the plants in remediation of heavy metal (Reinicke et al. 2013). Specifically, the metal-resistant actinomycetes have been reported to possess several traits that can alter heavy metal uptake by plants through acidification or by producing metal mobilizing/immobilizing substances. Experiments with Sorghum bicolor (sorghum) revealed that the inoculation of heavy metal-resistant Streptomyces mirabilis P16B-1 significantly increased the new tip growth and biomass of the sorghum plants as compared to the controls (Schutze et al. 2013). Similarly, Trivedi et al. (2007) demonstrated the potential of a psychrotrophic actinomycete Rhodococcus erythropolis to protect Pisum sativum (pea) from the toxicity of Cr in high concentrations and reported that this effect may be due to the reduction of Cr6+ to Cr3+ and various PGP traits such as the production of IAA, ACC deaminase activity, phosphate solubilization, and siderophore production. Khan et al. (2015) reported the greater potential of the Cr-resistant bacterium, Microbacterium arborescens HU33 associated with Prosopis juliflora, to protect ryegrass (Lolium multiflorum) from the toxicity of high concentrations of heavy metals such as Cr, Cd, Cu, Zn, and Pb grown on the tannery effluent contaminant soil. They attributed this effect to the ability of the bacterium to produce of IAA, siderophore, ACC deaminase, and solubilize P. Further, they reported that the inoculation of bacteria enhanced the heavy metal uptake of ryegrass plants. Javaid and Sultan (2012) reported that Streptomyces sp. isolated from the farmlands were shown to reduce toxic form of chromium [Cr(VI)] to less toxic form of Cr (III). This study suggests that by inoculating the plants with Cr-reducing actinomycetes, it should be possible to improve plant growth and Cr (VI) bioremediation.
An experiment with Arthrobacter creatinolyticus isolated from the rhizosphere of Spartina densiflora also revealed that the inoculation of microbial consortia along with A. creatinolyticus significantly increased the seed germination and plant growth under Cu and NaCl stress. In this case, enhanced plant growth could be correlated with various PGP traits such as N2 fixation and phosphate solubilization (Andrades-Moreno et al. 2014). Likewise, Wheeler et al. 2001 also observed that the inoculation of Frankia sp. significantly increased yield of their host Alnus glutinosa in the presence of Ni. Although previous studies have demonstrated a significant role of actinomycetes in facilitating the heavy metal uptake by plants, the molecular mechanisms involved in microbe-mediated heavy metal uptake by plants remain unknown. Moreover, there are some opposing viewpoints that the inoculation of actinomycetes reduced heavy metal accumulation in plants. For instance, Chatterjee et al. (2009) reported that the inoculation of Cr-reducing actinomycetes Cellulosimicrobium cellulans increased the plant growth and reduced Cr uptake in chilli plants. These contrasting effects may be due to microbial metal mobilization/immobilization potential, rhizosphere soil properties, the differences in the ability of plants to uptake heavy metals, metal toxicity, and its bioavailability.
14.7 Conclusions
The seriousness of heavy metal pollution in the environment dragged the attention of researchers toward sorting out of solutions for the removal of contaminants and a safer life. Though many conventional technologies have been employed, phytoremediation gains much importance because of its safe and eco-friendly method for remediation of these toxic heavy metals. Actinomycetes associated with the plant proved as a potential candidate in assisting phytoremediation. The metal-resistant beneficial actinomycetes not only improve the plant growth in metal-polluted soils but also protect their host plant from metal toxicity and alter heavy metal accumulation in plant tissues. The beneficial effects caused by actinomycetes indicate that inoculation with these microbes might have potential to improve phytoremediation efficiency in metal-contaminated soils. However, almost all the previous research on actinomycete-assisted phytoremediation were carried out in lab or greenhouse conditions; hence, further work including the interactions among actinomycetes, heavy metals, and plant is essential to apply this strategy in metal-polluted field level. Similarly, since the molecular background of mechanisms involved by actinomycetes in plant growth promotion and heavy metal uptake by plants is not yet been fully explored, more research has to be explored in order to make an actinomycete-assisted phytoremediation more effective.
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Taj, Z.Z., Rajkumar, M. (2016). Perspectives of Plant Growth-Promoting Actinomycetes in Heavy Metal Phytoremediation. In: Subramaniam, G., Arumugam, S., Rajendran, V. (eds) Plant Growth Promoting Actinobacteria. Springer, Singapore. https://doi.org/10.1007/978-981-10-0707-1_14
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