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3 Biotech

, Volume 5, Issue 2, pp 111–121 | Cite as

Phosphate-solubilizing bacteria-assisted phytoremediation of metalliferous soils: a review

  • Munees AhemadEmail author
Open Access
Review Article

Abstract

Heavy metal pollution of soils is of great concern. The presence of the toxic metal species above critical concentration not only harmfully affects human health but also the environment. Among existing strategies to remediate metal contaminates in soils, phytoremediation approach using metal accumulating plants is much convincing in terms of metal removal efficiency, but it has many limitations because of slow plant growth and decreased biomass owing to metal-induced stress. In addition, constrain of metal bioavailability in soils is the prime factor to restrict its applicability. Phytoremediation of metals in association with phosphate-solubilizing bacteria (PSB) considerably overcomes the practical drawbacks imposed by metal stress on plants. This review is an effort to describe mechanism of PSB in supporting and intensifying phytoremediation of heavy metals in soils and to address the developmental status of the current trend in application of PSB in this context.

Keywords

Bioremediation Heavy metals Hyperaccumulator plants Phosphate-solubilizing bacteria Phytoremediation Rhizobacteria 

Introduction

Soil is one of the most important natural resource on which lives of all plants, animals and microorganisms directly or indirectly dependent. In soils, different microorganisms thrive on abundantly present nutrients therein and through various interactions play a pivotal role in cycling of nutrients and pedogenesis (Ahemad and Khan 2013). Alteration or disturbance in soil ecosystem by added pollutants leads to substantial changes in functional activities of these important soil microorganisms (Swain and Abhijita 2013). Among pollutants, enormous amounts of toxic heavy metals such as chromium, cadmium, copper, zinc, mercury and lead contaminate soils through various geogenic, anthropogenic and technogenic activities (Ahemad 2012; Liu et al. 2013; Waterlot et al. 2013; Chodak et al. 2013). Due to non-biodegradable nature, metals in soils persist longer and pose a risk to human health through food chain because of their carcinogenicity, mutagenicity and teratogenicity (Ahemad and Malik 2011; Ali et al. 2013; Ahemad and Kibret 2013a). In addition, metals exceeding threshold limit affect microbial diversity and soil fertility (Huang et al. 2009). Thus, remediation of such metal-stressed soils is of paramount significance as they are rendered inappropriate for agricultural application.

Many physicochemical technologies are already in practice to clean up the metal-contaminated soils (Hashim et al. 2011). However, these conventional technologies are generally too costly to be applied to decontaminate the metal-polluted sites. Moreover, they generally adversely affect the texture and organic components, which are important to sustain the fertility of soils (Rajkumar et al. 2010). In view of sustainability issues and environmental ethics, bioremediation, the exploitation of biological processes for the cleanup of contaminated sites, is a promising, benign and ecologically sound alternative to chemical technologies (Hashim et al. 2011; Gillespie and Philp 2013). Among different bioremediation approaches, phytoremediation (utilizing metal accumulating plants to detoxify and extract contaminants in polluted soils) is gaining wide acceptance due to being cheap and environmentally safe but the major drawback of this technique is that it is time-consuming and high levels of metals decease the remediating efficiency of plants (Ali et al. 2013). Interestingly, interactions between plant and metal resistant bacteria have shown better remediation of heavy metals, and this synergism not only expedites the remediation process by ameliorating phytostabilization (reduction in metal toxicity through metal immobilization) and phytoextraction (metal accumulation as a result of metal mobilization) of metal species but also accelerate the plant growth and development (Khan et al. 2009).

Since last decades, several phosphate-solubilizing bacteria (PSB) exhibiting both heavy metal detoxifying traits and plant growth promoting activities have been explored and have been implicated in phytoremediation of metalliferous soils (He et al. 2010; Misra et al. 2012; Oves et al. 2013; Ahemad and Kibret 2013b). This review is an effort to emphasize how the beneficial association between plants and PSB can be used to remediate the metal-stressed soils efficiently. In this review, mechanism of PSB mediation in supporting and intensifying phytoremediation process is discussed in detail.

Phytoremediation: an overview

Currently, several physicochemical and biological techniques are in practice to remediate the metal-contaminated soils. Of them, remediation processes based upon the physicochemical parameters are very costly and also affect the soil properties, biodiversity and fertility. Different remediation technologies have been compared in Table 1 in terms of cost. It is obvious from the enlisted remediation approaches that phytoextraction (phytoremediation type) is one of the most cost effective method to remediate the metal-polluted soils (Padmavathiamma and Li 2007). Phytoremediation occurs only at marginal cost, which is due to harvesting and field management, e.g., weed control. In addition, the resulting biomass of phytoremediating plants can be used for heat and energy production in specialized facilities (Peuke and Rennenberg 2005). Unlike physicochemical processes, phytormediation is an eco-friendly and comprehensive strategy having no side effects on soil texture and health (Suresh and Ravishankar 2004).
Table 1

Cost of different remediation technologies

Process

Cost (US$/ton)

Other factors

Vitrification

75–425

Long-term monitoring

Land filling

100–500

Transport/excavation/monitoring

Chemical treatment

100–500

Recycling of contaminants

Electrokinetics

20–200

Monitoring

Phytoextraction

5–40

Disposal of phytomass

Source: Glass (1999)

In phytoextraction, metals are accumulated in plant biomass from moderately contaminated soils. On the other hand, phytostabilization is a long-term, in situ approach applicable in polymetallic soils wherein concentration and the area of metal contaminant are so extensive that phytoextraction cannot work; therefore, metals are not allowed to enter plants but are captured in situ through biosorption, precipitation or reducing toxicity (de-Bashan et al. 2012). Plants selected for phytostabilization must be metal-tolerant (metallophytes) and should not accumulate metals into root tissues. Despite having mechanisms to evade metal translocation in shoot tissues, considerable amount of metals may be found in the shoot parts. Metal accumulation in plants can measured in terms of (1) bioconcentration factor (BF)/accumulation factor (AF) which is the ratio of metal concentration in the shoot tissue to the soils and (2) translocation factor (TF) which is the ratio of metals in shoot to those in root. For better phytostabilization, these values should preferably be ≪1 while the values must be ≫1 in addition to higher plant biomass for an ideal phytoextracting plants (Peuke and Rennenberg 2005; Mendez and Maier 2008).

Phosphate-solubilizing bacteria

After nitrogen, phosphorus (P) is the second essential macronutrient for plant growth and development. Generally, substantial amount of phosphorus (P) occurs in soil ranging from 400 to 1,200 mg/kg of soil, either in mineral forms, e.g., apatite, hydroxyapatite and oxyapatite, or organic forms such as, inositol phosphate (soil phytate), phosphomonoesters, phosphodiesters and phosphotriesters (Ahemad et al. 2009). However, the concentration of soluble forms of P in soil is usually ~1 mg/kg or less (Goldstein 1994). In addition, it has a very limited bioavailability to growing plants due to high reactivity of phosphate ions in soils. To circumvent this deficiency, phosphatic fertilizers are applied in soils. But most of the applied P in the forms of fertilizers is precipitated; consequently, a very small fraction is available for absorption by plants. As an eco-friendly and economical alternative to provide substantial amount of soluble P to plants for growth promotion is the exploitation of P solubilization and mineralization traits of PSB.

Additionally, PSB not only protect plants from phytopathogens through the production of antibiotics, HCN, phenazines and antifungal metabolites, etc. (Upadhayay and Srivastava 2012; Singh et al. 2013), but also promote plant growth through N2 fixation (He et al. 2010), siderophore production (Ahemad and Khan 2012a, b), phytohormone secretion (Misra et al. 2012; Oves et al. 2013) and lowering ethylene levels (Jiang et al. 2008; Kumar et al. 2009) (Fig. 1).
Fig. 1

Mechanisms of phosphate-solubilizing bacteria-mediated plant growth promotion. ROS reactive oxygen species, ACC 1-aminocyclopropane-1-carboxylate, NH 3 ammonia, HCN hydrogen cyanate, IAA indole-3-acetic acid, P phosphate

Mechanisms of PSB-assisted metal phytoremediation

Although decontamination of metal-polluted soils using plants (phytoextraction/phytostabilization) has shown encouraging results, this approach has limitations in case of the polluted sites wherein metal concentration is extremely elevated (Gamalero and Glick 2012). Under high metal stress, their physiological activities are hampered; growth and development are severely impeded; and resistance mechanisms are weakened, and in turn, they become prone to phyto-pathogen attacks (Ma et al. 2011c). Further, their metal phytoremediating efficiency is depressingly affected, and the process of metal decontamination is proportionally impeded depending upon several factors (Martin and Ruby 2004). Intended to overcome the noxious level of metals that significantly decline the plant growth, PSB with multiple plant growth promoting traits (Table 2; Fig. 1) and concurrent metal detoxifying potentials (Fig. 2) may increase the phytoremediation competence of plants by promoting their growth and health even under hazardous levels of different metals. As adjuncts with plants, PSB remediate metal-contaminated soils largely through facilitating either phytostabilization (decreasing metal toxicity by transforming metal species into immobile forms) or phytoextraction (metal mobilization and accumulation in plant tissues) (Fig. 3). Various plant growth promoting traits of PSB, such as organic acid production, secretion of siderophores, IAA production and ACC deaminase activity, contribute in enhancing the phytoremediation capability of plants.
Table 2

Plant growth promoting substances released by phosphate-solubilizing bacteria

PGPR

Plant growth promoting traits

References

Pseudomonas aeruginosa strain OSG41

IAA, siderophores

Oves et al. (2013)

Pseudomonas sp.

IAA, HCN

Singh et al. (2013)

Acinetobacter haemolyticus RP19

IAA

Misra et al. (2012)

Pseudomonas putida

IAA, siderophores, HCN, ammonia

Ahemad and Khan (2011c, 2012b, c)

Pseudomonasfluorescens strain Psd

IAA, siderophores, HCN, antibiotics, biocontrol activity

Upadhayay and Srivastava (2012)

Bacillus thuringiensis

IAA

Sandip et al. (2011)

Pseudomonas aeruginosa

IAA, siderophores, HCN, ammonia

Ahemad and Khan (2010c, 2011a, e, 2012d)

Pseudomonas sp. TLC 6-6.5-4

IAA, siderophore

Li and Ramakrishna (2011)

Bacillus sp.

IAA, HCN

Karuppiah and Rajaram (2011)

Klebsiella sp.

IAA, siderophores, HCN, ammonia

Ahemad and Khan (2011b, d, 2012a)

Enterobacter asburiae

IAA, siderophores, HCN, ammonia

Ahemad and Khan (2010a, b)

Bacillus species PSB10

IAA, siderophores, HCN, ammonia

Wani and Khan (2010)

Arthrobacter sp. MT16, Microbacterium sp. JYC17, Pseudomonaschlororaphis SZY6, Azotobactervinelandii GZC24, Microbacteriumlactium YJ7

ACC deaminase, IAA, siderophore

He et al. (2010)

Pseudomonas sp.

IAA, siderophore, HCN, biocontrol potentials

Tank and Saraf (2009)

Enterobacteraerogenes NBRI K24, Rahnellaaquatilis NBRI K3

ACC deaminase, IAA, siderophore

Kumar et al. (2009)

Enterobacter sp.

ACC deaminase, IAA, siderophore

Kumar et al. (2008)

Burkholderia

ACC deaminase, IAA, siderophore

Jiang et al. (2008)

Pseudomonas aeruginosa

ACC deaminase, IAA, siderophore

Ganesan (2008)

ACC 1-aminocyclopropane-1-carboxylate, HCN hydrogen cyanate, IAA indole-3-acetic acid

Fig. 2

Various bacterial interactions with heavy metals in metal-polluted soils: 1 precipitation/crystallization of metals occurs due to bacteria-mediated reactions or as a result of the production of specific metabolites. 2 Plasmid-DNA-encoded efflux transporters (e.g., ATPase pumps or chemiosmotic ion/proton pumps) expel the accumulated metals outside the cell. 3 Metals bind to the anionic functional groups (e.g., sulfhydryl, carboxyl, hydroxyl, sulfonate, amine and amide groups) of extracellular materials present on cell surfaces. 4 Organic acids secreted by bacteria solubilize the insoluble metal minerals. 5 Some bacteria utilize methylation as an alternative for metal resistance/detoxification mechanism, which involves the transfer of methyl groups to metals and metalloids. 6 Metals enter the bacterial cell by chromosomal DNA-encoded metal transporters either through ATP hydrolysis or as a result of chemiosmotic gradient across the cytoplasmic membrane. 7 Bacterial cell also accumulate substantial concentration of metals by the synthesis of low molecular mass cysteine-rich metal-binding proteins, metallothioneins having high affinities for several metals. 8 Membrane-embedded metal reductases, generally encoded by chromosomal DNA, reduce metals in the presence of electron donors. 9 Siderophore secretion decreases metal bioavailability by binding metal ions having chemistry similar to iron. 10 Superoxide dismutase, catalase and glutathione are activated to combat oxidative stress produced by the reactive oxygen species (ROS), and DNA repair system is activated to repair the DNA damaged due to various metal interactions within cell

Fig. 3

Schematic portrayal of the role of metal resistant phosphate-solubilizing bacteria in alleviation of heavy metal toxicity, phytoextraction and phytostabilization

Organic acids

In most of the metalliferous soils, metals are strongly adhered to soil particles; therefore, they are not easily available for uptake by phytoextracting plants (Gamalero and Glick 2012). In this context, PSB are very promising agents since they solubilize the insoluble and biologically unavailable metals such as Ni (Becerra-Castro et al. 2011), Cu (Li and Ramakrishna 2011) and Zn (He et al. 2013) by secreting low molecular weight organic acids; thus, they facilitate metal bioavailability for plant uptake (Becerra-Castro et al. 2011). A number of organic acids such as lactic, citric, 2-ketogluconic, malic, glycolic, oxalic, malonic, tartaric, valeric, piscidic, succinic and formic have been identified, which have chelating properties (Panhwar et al. 2013). Moreover, metal bioavailability in metal-stressed soils can be further increased by inoculating biosurfactant producing PSB as the bacterial biosurfactants aid in metal release from soil particles (Gamalero and Glick 2012; Singh and Cameotra 2013).

Siderophores

Generally, iron occurs mainly as Fe3+ and forms insoluble hydroxides and oxyhydroxides, thus is not easily available to both plants and microorganisms (Ahemad and Kibret 2013b). Under iron-limiting conditions to acquire iron, bacteria secret low molecular weight siderophores, which are iron chelators with exceptionally strong affinity for ferric iron (Fe3+) (Schalk et al. 2011). Despite their preferential affinity for Fe3+, they can also chelate several other metals such as, magnesium, manganese, chromium (III), gallium (III), cadmium, zinc, copper, nickel, arsenic and lead, and radionuclides, including plutonium (IV) with variable affinities (Nair et al. 2007; Rajkumar et al. 2010; Schalk et al. 2011). Supply of iron to growing plants under heavy metal pollution becomes more important as bacterial siderophores help to minimize the stress imposed by metal contaminants (Gamalero and Glick 2012). For instance, siderophore overproducing mutant NBRI K28 SD1 of phosphate-solubilizing bacterial strain Enterobacter sp. NBRI K28 not only increased plant biomass but also enhanced phytoextraction of Ni, Zn and Cr by Brassicajuncea (Indian mustard) (Kumar et al. 2008).

Indole acetic acid

Phytohormone, indole-3-acetic acid (IAA) whose biosynthesis requires l-tryptophan as a precursor, is the most important auxin, which regulates several morphological and physiological functions in plants (Glick 2012). Although it has been implicated in stimulation of root growth, alleviation of salt stress, plant-pathogen interactions, legume-rhizobia interactions and eliciting induced systemic resistance against various diseases, it primarily is involved in stimulating the proliferation of lateral roots in plants, thereby root surface area is increased and they absorb more water and soil minerals (Egamberdieva 2009; Lugtenberg and Kamilova 2009, Ahemad and Kibret 2013b). Many phosphate-solubilizing bacterial genera (He et al. 2010; Ahemad and Khan 2011a, 2012b; Misra et al. 2012; Oves et al. 2013) in soils have been reported to secret IAA that is absorbed by plant roots to increase the endogenous pool of plant IAA (Glick et al. 2007). However, effects of variable IAA concentrations vary among different plant species. Moreover, optimum concentration of bacterial IAA has stimulatory effect, while high concentration (supra-optimal) of those is inhibitory to root growth (Glick 2012).

Generally, bacterial IAA facilitates adaptation of host plants in metal-contaminated sites through triggering physiological changes in plant cell metabolism under metal stress so that the growing plants can withstand high concentrations of heavy metals (Glick 2010). However, Hao et al. (2012) determined that bacterial IAA had a larger impact on the growth of host plants under metal stress rather than bacterial metal resistance through transposon mutagenesis in phosphate-solubilizing Agrobacterium tumefaciens CCNWGS0286.

1-Aminocyclopropane-1-carboxylate (ACC) deaminase

Another phytohormone, ethylene, modulates many important physiological activities of growing plants including root growth and development. Under both biotic (e.g., phyto-pathogen attacks) and abiotic (e.g., heavy metals, drought, flooding and salinity) stresses, plant produces ethylene up to the level that is inhibitory to root growth (Khalid et al. 2006; Arshad et al. 2007; Nadeem et al. 2007, 2009; Chen et al. 2013). Since phytoremediation approach to decontaminate the metal-spiked soils is largely reliant on the profuse growth of roots and the efficient uptake and mobilization of heavy metal ions via prolific root system to different plant parts, stress-induced ethylene at supra-optimal concentration leads to reduced root growth in turn, limiting the proficiency of metal remediating plants (Arshad et al. 2007; Gamalero and Glick 2012).

To counter this physiological crisis, an enzyme ACC deaminase (EC 4.1.99.4) produced by many soil microflora including PSB (Kumar et al. 2009; He et al. 2010), degrades ACC (an immediate precursor for ethylene in plants) into 2-oxobutanoate and ammonia hence decreases the ethylene biosynthesis in plant tissues (Saleem et al. 2007; Shaharoona et al. 2007; Zahir et al. 2009). Ammonia released in this way is utilized by ACC deaminase-expressing organisms as nitrogen source for growth (Glick 2005). In addition, while attached with the plant roots, ACC deaminase-containing bacteria act as a sink for ACC ensuring that ethylene level may not increased to the point where root growth and development is impaired (Glick 1995). Thus, bacterial ACC deaminase-induced extensive root proliferation in metal remediating (hyperaccumulator) plants results into efficient phytoremediation processes in metal-polluted soils (Arshad et al. 2007). Several species of ACC deaminase-containing PSB have been isolated and successfully improved the plant growth under metal stress (Ganesan 2008; Jiang et al. 2008; Sun et al. 2009).

Exploiting PSB in phytoremediation of metal-stressed soils

In various studies, growth promoting effects of PSB are well established both in unpolluted and polluted soils when used as inoculants (Ma et al. 2011a, b; Oves et al. 2013). However, degree of their impact on different plants varies depending upon plant species, bacterial species, soil types and environmental factors. In metalliferous soils, several authors have studied phytoremediation using PSB as bioinoculants to remove different heavy metals from soils. Worldwide, the research in this direction is currently being carried out considering various aspects to overcome hurdles which impede the efficient removal of metal contaminants. In Table 3, various phytoremediation studies have been listed to show effects of different PSB using different plant species and metals. Many insights can be drawn following analyses of these studies:
Table 3

Phosphate-solubilizing bacteria (PSB) mediated metal remediation and plant growth promotion

PSB

Plant

Heavy metals

Conditions

Role of PSB (Mode of metal remediation)

References

Pseudomonas aeruginosa strain OSG41

Chickpea (Cicerarietinum)

Cr

Pots

Increased the dry matter, symbiotic traits, grain yield and grain protein of chickpea plants in the presence of chromium and decreased the uptake of chromium by 36, 38 and 40 % in roots, shoots and grains, respectively

(Phytostabilization)

Oves et al. (2013)

Acinetobacter haemolyticus RP19

Pearl millet (Pennisetum glaucum)

Zn

Pots

Increased significantly root length, shoot length, fresh weight and root biomass

(Phytostabilization)

Misra et al. (2012)

Pseudomonas sp. A3R3

Alyssumserpyllifolium, Brassicajuncea

Ni

Pots

Increased significantly the biomass (B. juncea) and Ni content (A. serpyllifolium) in plants grown in Ni-stressed soil

(Phytoextraction)

Ma et al. (2011a)

Pseudomonas sp. TLC 6-6.5-4

Zeamays, Helianthusannuus

Cu

Pots

Significantly increased copper uptake by plants and also enhanced the biomass of maize

(Phytoextraction)

Li and Ramakrishna (2011)

Psychrobacter sp. SRS8

Ricinuscommunis, Helianthusannuus

Ni

Pots

Stimulated plant growth and Ni accumulation in both plant species with increased plant biomass, chlorophyll and protein content

(Phytoextraction)

Ma et al. (2011b)

Arthrobacter sp. MT16, Microbacterium sp. JYC17, Pseudomonaschlororaphis SZY6, Azotobactervinelandii GZC24, Microbacteriumlactium YJ7

Brassica napus

Cu

Gnotobiotic condition

Increased (16–41 %) root length (Phytoextraction)

He et al. (2010)

Bacillus species PSB10

Chickpea (Cicerarietinum)

Cr

Pots

Significantly improved growth, nodulation, chlorophyll, leghemoglobin, seed yield and grain protein and reduced the uptake of chromium in roots, shoots and grains

(Phytostabilization)

Wani and Khan (2010)

Pseudomonas sp. SRI2, Psychrobacter sp. SRS8, Bacillus sp. SN9

Brassicajuncea, Brassicaoxyrrhina

Ni

Pots

Increased the biomass of the test plants and enhanced Ni accumulation in plant tissues

(Phytoextraction)

Ma et al. (2009a)

Psychrobacter sp. SRA1, Bacilluscereus SRA10

Brassicajuncea, Brassicaoxyrrhina

Ni

Pots

Enhanced the metal accumulation in plant tissues by facilitating the release of Ni from the non-soluble phases in the soil

(Phytoextraction)

Ma et al. (2009b)

Achromobacter xylosoxidans strain Ax10

Brassica juncea

Cu

Pots

Significantly improved Cu uptake by plants and increased the root length, shoot length, fresh weight and dry weight of plants

(Phytoextraction)

Ma et al. (2009c)

Pseudomonas sp.

Chickpea

Ni

Pots

Enhanced fresh and dry weight of plants even at 2 mM nickel concentration

(Phytostabilization)

Tank and Saraf (2009)

Enterobacteraerogenes NBRI K24, Rahnellaaquatilis NBRI K3

Brassica juncea

Ni, Cr

Pots

Increased plant root length, dry weight, leaf protein and chlorophyll content with Ni and Cr uptake

(Phytostabilization)

Kumar et al. (2009)

Bacillusweihenstephanensis strain SM3

Helianthus annuus

Ni, Cu, Zn

Pots

Increased plant biomass and the accumulation of Cu and Zn in the root and shoot systems, also augmented the concentrations of water soluble Ni, Cu and Zn in soil with their metal mobilizing potential

(Phytoextraction)

Rajkumar et al. (2008)

Pseudomonasaeruginosa strain MKRh3

Black gram

Cd

Pots

Plants showed lessened cadmium accumulation, extensive rooting, and enhanced plant growth

(Phytostabilization)

Ganesan (2008)

Enterobacter sp. NBRI K28, mutant NBRI K28 SD1

Brassica juncea

Ni, Cr, Zn

Pots

Improved plant growth parameters such as biomass, chlorophyll and protein and increased Ni, Cr and Zn uptake

(Phytoextraction)

Kumar et al. (2008)

Burkholderia sp. J62

Lycopersicon esculentum

Pb, Cd

Pots

Increased root and shoot dry weight as well as Pb and Cd uptake

(Phytoextraction)

Jiang et al. (2008)

Bacillussubtilis SJ-101

Brassica juncea

Ni

Growth chamber

Facilitated Ni accumulation

(Phytoextraction)

Zaidi et al. (2006)

Pseudomonas sp., Bacillus sp.

Mustard

Cr

Pots

Stimulated plant growth and decreased Cr(VI) content

(Phytostabilization)

Rajkumar et al. (2006)

Pseudomonas fluorescens

Soybean

Hg

Greenhouse

Increased plant growth

(Phytostabilization)

Gupta et al. (2005)

Pseudomonas sp.

Soybean, mungbean, wheat

Ni, Cd, Cr

Pots

Promotes growth of plants

(Phytostabilization)

Gupta et al. (2002)

1. Most of the laboratory or green house studies have employed plants of Brassicaseae family in conjunction with PSB because plant species of this family (hyperaccumulator plants) have been reported to accumulate substantial amount of metals in their tissues.

2. Diverse species of PSB have been used in these metal phytoremediation studies. However, species like Pseudomonasaeruginosa, being an opportunistic human pathogen, poses a challenge to be released in the soil environment (Walker et al. 2004). Hence, ethical and juridical considerations are needed if they are to be used as inoculants in fields.

3. Among environmentally toxic metals, only few metals such as, Ni, Cu, Zn and Cr have been studied extensively while other toxicologically important metals, e.g., As, Cd, Hg and Pb are least considered. Therefore, phytoremediation studies concerning other metals would reveal new challenges, insights and problems leading to pave ways for further research in this course.

4. Both approaches of metal remediation, phytostabilization and phytoextraction have been implicated in these studies. As the plants growing in metal-stressed soils are weakened due to metal-induced physiological damage, they become prone to diseases and pests attack. In practicing phytoextraction strategy, it is paramount important that selected plants must exhibit resistance to phytopathogens in order to smoothly function in metal-stressed soils. Moreover, further exploration and application of PSB strains, possessing additional traits which confer resistance to plants against various diseases, would be a better choice for metal phytoextraction.

Conclusions

Efficiency of phytoremediation of metal-polluted soils is chiefly determined by the metal bioavailability which in turn increases the metal uptake by plants. Hence, PSB compared with other plant growth promoting bacteria would be marvelous alternatives to boost this process as organic acids, and bio-surfactants secreted by these organisms solubilize sparingly soluble metal complexes, consequently increase bioavailability of metals and nutrient supply to soils. Thus, PSB with multifunctional activities (such as production of siderophore, IAA, ACC deaminase, organic acids and anti-pathogen metabolites) are better choice in assisting the phytoremediation process in metal-contaminated soils.

Notes

Conflict of interest

The authors declare that there is no conflict of interests.

References

  1. Ahemad M (2012) Implications of bacterial resistance against heavy metals in bioremediation: a review. IIOABJ 3:39–46Google Scholar
  2. Ahemad M, Khan MS (2010a) Influence of selective herbicides on plant growth promoting traits of phosphate solubilizing Enterobacter asburiae strain PS2. Res J Microbiol 5:849–857CrossRefGoogle Scholar
  3. Ahemad M, Khan MS (2010b) Plant growth promoting activities of phosphate-solubilizing Enterobacter asburiae as influenced by fungicides. Eur Asian J Biosci 4:88–95CrossRefGoogle Scholar
  4. Ahemad M, Khan MS (2010c) Phosphate-solubilizing and plant-growth-promoting Pseudomonasaeruginosa PS1 improves greengram performance in quizalafop-p-ethyl and clodinafop amended soil. Arch Environ Contam Toxicol 58:361–372CrossRefGoogle Scholar
  5. Ahemad M, Khan MS (2011a) Toxicological assessment of selective pesticides towards plant growth promoting activities of phosphate solubilizing Pseudomonasaeruginosa. Acta Microbiol Immunol Hung 58:169–187CrossRefGoogle Scholar
  6. Ahemad M, Khan MS (2011b) Effects of insecticides on plant-growth-promoting activities of phosphate solubilizing rhizobacterium Klebsiella sp. strain PS19. Pestic Biochem Physiol 100:51–56CrossRefGoogle Scholar
  7. Ahemad M, Khan MS (2011c) Assessment of plant growth promoting activities of rhizobacterium Pseudomonasputida under insecticide-stress. Microbiol J 1:54–64CrossRefGoogle Scholar
  8. Ahemad M, Khan MS (2011d) Toxicological effects of selective herbicides on plant growth promoting activities of phosphate solubilizing Klebsiella sp. strain PS19. Curr Microbiol 62:532–538CrossRefGoogle Scholar
  9. Ahemad M, Khan MS (2011e) Pseudomonasaeruginosa strain PS1 enhances growth parameters of greengram [Vignaradiata (L.) Wilczek] in insecticide-stressed soils. J Pest Sci 84:123–131CrossRefGoogle Scholar
  10. Ahemad M, Khan MS (2012a) Biotoxic impact of fungicides on plant growth promoting activities of phosphate-solubilizing Klebsiella sp. isolated from mustard (Brassica compestris) rhizosphere. J Pest Sci 85:29–36CrossRefGoogle Scholar
  11. Ahemad M, Khan MS (2012b) Effect of fungicides on plant growth promoting activities of phosphate solubilizing Pseudomonas putida isolated from mustard (Brassica compestris) rhizosphere. Chemosphere 86:945–950CrossRefGoogle Scholar
  12. Ahemad M, Khan MS (2012c) Evaluation of plant growth promoting activities of rhizobacterium Pseudomonasputida under herbicide-stress. Ann Microbiol 62:1531–1540CrossRefGoogle Scholar
  13. Ahemad M, Khan MS (2012d) Alleviation of fungicide-induced phytotoxicity in greengram [Vignaradiata (L.) Wilczek] using fungicide-tolerant and plant growth promoting Pseudomonas strain. Saudi J Biol Sci 19:451–459CrossRefGoogle Scholar
  14. Ahemad M, Khan MS (2013) Pesticides as antagonists of rhizobia and the legume-Rhizobium symbiosis: a paradigmatic and mechanistic outlook. Biochem Mole Biol 1:63–75CrossRefGoogle Scholar
  15. Ahemad M, Kibret M (2013a) Recent trends in microbial biosorption of heavy metals: a review. Biochem Mol Biol 1:19–26CrossRefGoogle Scholar
  16. Ahemad M, Kibret M (2013b) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci. doi: 10.1016/j.jksus.2013.05.001
  17. Ahemad M, Malik A (2011) Bioaccumulation of heavy metals by zinc resistant bacteria isolated from agricultural soils irrigated with wastewater. Bacteriol J 2:12–21CrossRefGoogle Scholar
  18. Ahemad M, Zaidi A, Khan MS, Oves M (2009) Biological importance of phosphorus and phosphate solubilizing microbes. In: Khan MS, Zaidi A (eds) Phosphate solubilizing microbes for crop improvement. Nova Science Publishers Inc., New York, pp 1–14Google Scholar
  19. Ali H, Khan E, Anwar SM (2013) Phytoremediation of heavy metals-concepts and applications. Chemosphere 91:869–881CrossRefGoogle Scholar
  20. Arshad M, Saleem M, Hussain S (2007) Perspectives of bacterial ACC deaminase in phytoremediation. Trends Biotechnol 25:356–362CrossRefGoogle Scholar
  21. Becerra-Castro C, Prieto-Fernández A, Alvarez-Lopez V, Monterroso C, Cabello-Conejo MI, Acea MJ, Kidd PS (2011) Nickel solubilizing capacity and characterization of rhizobacteria isolated from hyperaccumulating and non-hyperaccumulating subspecies of Alyssumserpyllifolium. Int J Phytoremediat 1:229–244CrossRefGoogle Scholar
  22. Chen L, Dodd IC, Theobald JC, Belimov AA, Davies WJ (2013) The rhizobacterium Variovorax paradoxus 5C-2, containing ACC deaminase, promotes growth and development of Arabidopsis thaliana via an ethylene-dependent pathway. J Exp Bot. doi: 10.1093/jxb/ert031Google Scholar
  23. Chodak M, Gołębiewski M, Morawska-Płoskonka J, Kuduk K, Niklińska M (2013) Diversity of microorganisms from forest soils differently polluted with heavy metals. Appl Soil Ecol 64:7–14CrossRefGoogle Scholar
  24. de-Bashan LE, Hernandez JP, Bashan Y (2012) The potential contribution of plant growth-promoting bacteria to reduce environmental degradation—a comprehensive evaluation. Appl Soil Ecol 61:171–189CrossRefGoogle Scholar
  25. Egamberdieva D (2009) Alleviation of salt stress by plant growth regulators and IAA producing bacteria in wheat. Acta Physiol Plant 31:861–864CrossRefGoogle Scholar
  26. Gamalero E, Glick BR (2012) Plant growth-promoting bacteria and metals phytoremediation. In: Anjum NA, Pereira ME, Ahmad I, Duarte AC, Umar S, Khan NA (eds) Phytotechnologies: remediation of environmental contaminants. CRC Press, Boca Raton, pp 361–376CrossRefGoogle Scholar
  27. Ganesan V (2008) Rhizoremediation of cadmium soil using a cadmium-resistant plant growth-promoting rhizopseudomonad. Curr Microbiol 56:403–407CrossRefGoogle Scholar
  28. Gillespie IMM, Philp JC (2013) Bioremediation, an environmental remediation technology for the bioeconomy. Trends Biotechnol. doi: 10.1016/j.tibtech.2013.01.015Google Scholar
  29. Glass DJ (1999) U.S. and international markets for phytoremediation, 1999–2000. D. Glass Associates, Needham, p 266Google Scholar
  30. Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117CrossRefGoogle Scholar
  31. Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251:1–7CrossRefGoogle Scholar
  32. Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374CrossRefGoogle Scholar
  33. Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Hindawi Publishing Corporation, ScientificaGoogle Scholar
  34. Glick BR, Todorovic B, Czarny J, Cheng Z, Duan J, McConkey B (2007) Promotion of plant growth by bacterial ACC deaminase. Crit Rev Plant Sci 26:227–242CrossRefGoogle Scholar
  35. Goldstein AH (1994) Involvement of the quinoprotein glucose dehydrogenase in the solubilization of exogenous phosphates by gram-negative bacteria. In: Torriani-Gorini A, Yagil E, Silver S (eds) Phosphate in microorganisms: cellular and molecular biology. ASM, Washington, DC, pp 197–203Google Scholar
  36. Gupta A, Meyer JM, Goel R (2002) Development of heavy metal resistant mutants of phosphate solubilizing Pseudomonas sp. NBRI4014 and their characterization. Curr Microbiol 45:323–332CrossRefGoogle Scholar
  37. Gupta A, Rai V, Bagdwal N, Goel R (2005) In situ characterization of mercury resistant growth promoting fluorescent pseudomonads. Microbiol Res 160:385–388CrossRefGoogle Scholar
  38. Hao X, Xie P, Johnstone L, Miller SJ, Rensing C, Weia G (2012) Genome sequence and mutational analysis of plant-growth-promoting bacterium Agrobacterium tumefaciens CCNWGS0286 isolated from a zinc-lead mine tailing. Appl Environ Microbiol 78:5384–5394CrossRefGoogle Scholar
  39. Hashim MA, Mukhopadhyay S, Sahu JN, Sengupta B (2011) Remediation technologies for heavy metal contaminated groundwater. J Environ Manag 92:2355–2388CrossRefGoogle Scholar
  40. He LY, Zhang YF, Ma HY, Su LN, Chen ZJ, Wang QY, Meng Q, Fang SX (2010) Characterization of copper resistant bacteria and assessment of bacterial communities in rhizosphere soils of copper-tolerant plants. Appl Soil Ecol 44:49–55CrossRefGoogle Scholar
  41. He H, Ye Z, Yang D, Yan J, Xiao L, Zhong T, Yuan M, Cai X, Fang Z, Jing Y (2013) Characterization of endophytic Rahnella sp. JN6 from Polygonumpubescens and its potential in promoting growth and Cd, Pb, Zn uptake by Brassica napus. Chemosphere 90:1960–1965CrossRefGoogle Scholar
  42. Huang S, Peng B, Yang Z, Chai L, Zhou L (2009) Chromium accumulation, microorganism population and enzyme activities in soils around chromium-containing slag heap of steel alloy factory. Trans Nonferrous Met Soc China 19:241–248CrossRefGoogle Scholar
  43. Jiang CY, Sheng XF, Qian M, Wang QY (2008) Isolation and characterization of a heavy metal resistant Burkholderia sp. from heavy metal-contaminated paddy field soil and its potential in promoting plant growth and heavy metal accumulation in metal polluted soil. Chemosphere 72:157–164CrossRefGoogle Scholar
  44. Karuppiah P, Rajaram S (2011) Exploring the potential of chromium reducing Bacillus sp. and there plant growth promoting activities. J Microbiol Res 1:17–23CrossRefGoogle Scholar
  45. Khalid A, Akhtar MJ, Mahmood MH, Arshad M (2006) Effect of substrate-dependent microbial ethylene production on plant growth. Microbiology 75:231–236CrossRefGoogle Scholar
  46. Khan MS, Zaidi A, Wani PA, Oves M (2009) Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environ Chem Lett 7:1–19CrossRefGoogle Scholar
  47. Kumar KV, Singh N, Behl HM, Srivastava S (2008) Influence of plant growth promoting bacteria and its mutant on heavy metal toxicity in Brassica juncea grown in fly ash amended soil. Chemosphere 72:678–683CrossRefGoogle Scholar
  48. Kumar KV, Srivastava S, Singh N, Behl HM (2009) Role of metal resistant plant growth promoting bacteria in ameliorating fly ash to the growth of Brassicajuncea. J Hazard Mater 170:51–57CrossRefGoogle Scholar
  49. Li K, Ramakrishna W (2011) Effect of multiple metal resistant bacteria from contaminated lake sediments on metal accumulation and plant growth. J Hazard Mater 189:531–539CrossRefGoogle Scholar
  50. Liu M, Huang B, Bi X, Ren Z, Shenga G, Fu J (2013) Heavy metals and organic compounds contamination in soil from an e-waste region in South China. Environ Sci Process Impacts 15:919–929CrossRefGoogle Scholar
  51. Lugtenberg B, Kamilova F (2009) Plant growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556CrossRefGoogle Scholar
  52. Ma Y, Rajkumar M, Freitas H (2009a) Isolation and characterization of Ni mobilizing PGPB from serpentine soils and their potential in promoting plant growth and Ni accumulation by Brassica spp. Chemosphere 75:719–725CrossRefGoogle Scholar
  53. Ma Y, Rajkumar M, Freitas H (2009b) Improvement of plant growth and nickel uptake by nickel resistant-plant-growth promoting bacteria. J Hazard Mater 166:1154–1161CrossRefGoogle Scholar
  54. Ma Y, Rajkumar M, Freitas H (2009c) Inoculation of plant growth promoting bacterium Achromobacterxylosoxidans strain Ax10 for the improvement of copper phytoextraction by Brassicajuncea. J Environ Manag 90:831–837CrossRefGoogle Scholar
  55. Ma Y, Prasad MNV, Rajkumar M, Freitas H (2011a) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29:248–258CrossRefGoogle Scholar
  56. Ma Y, Rajkumar M, Luo Y, Freitas H (2011b) Inoculation of endophytic bacteria on host and non-host plants-effects on plant growth and Ni uptake. J Hazard Mater 195:230–237CrossRefGoogle Scholar
  57. Ma Y, Rajkumar M, Vicente JA, Freitas H (2011c) Inoculation of Ni-resistant plant growth promoting bacterium Psychrobacter sp. strain SRS8 for the improvement of nickel phytoextraction by energy crops. Int J Phytoremediat 13:126–139CrossRefGoogle Scholar
  58. Martin TA, Ruby MV (2004) Review of in situ remediation technologies for lead, zinc, and cadmium in soil. Remediat Summer. doi: 10.1002/rem.20011Google Scholar
  59. Mendez MO, Maier RM (2008) Phytostabilization of mine tailings in arid and semiarid environments-an emerging remediation technology. Environ Health Perspect 116:278–283CrossRefGoogle Scholar
  60. Misra N, Gupta G, Jha PN (2012) Assessment of mineral phosphate-solubilizing properties and molecular characterization of zinc-tolerant bacteria. J Basic Microbiol 52:549–558CrossRefGoogle Scholar
  61. Nadeem SM, Zahir ZA, Naveed M, Arshad M (2007) Preliminary investigations on inducing salt tolerance in maize through inoculation with rhizobacteria containing ACC deaminase activity. Can J Microbiol 53:1141–1149CrossRefGoogle Scholar
  62. Nadeem SM, Zahir ZA, Naveed M, Arshad M (2009) Rhizobacteria containing ACC-deaminase confer salt tolerance in maize grown on salt-affected fields. Can J Microbiol 55:1302–1309CrossRefGoogle Scholar
  63. Nair A, Juwarkar AA, Singh SK (2007) Production and characterization of siderophores and its application in arsenic removal from contaminated soil. Water Air Soil Pollut 180:199–212CrossRefGoogle Scholar
  64. Oves M, Khan MS, Zaidi A (2013) Chromium reducing and plant growth promoting novel strain Pseudomonasaeruginosa OSG41 enhance chickpea growth in chromium amended soils. Eur J Soil Biol 56:72–83CrossRefGoogle Scholar
  65. Padmavathiamma PK, Li LY (2007) Phytoremediation technology: hyper-accumulation metals in plants. Water Air Soil Pollut 184:105–126CrossRefGoogle Scholar
  66. Panhwar QA, Jusop S, Naher UA, Othman R, Razi MI (2013) Application of potential phosphate-solubilizing bacteria and organic acids on phosphate solubilization from phosphate rock in aerobic rice. Sci World J. doi: 10.1155/2013/272409Google Scholar
  67. Peuke AD, Rennenberg H (2005) Phytoremediation. EMBO Rep 6:497–501CrossRefGoogle Scholar
  68. Rajkumar M, Nagendran R, Kui JL, Wang HL, Sung ZK (2006) Influence of plant growth promoting bacteria and Cr(VI) on the growth of Indian mustard. Chemosphere 62:741–748CrossRefGoogle Scholar
  69. Rajkumar M, Ma Y, Freitas H (2008) Characterization of metal-resistant plant-growth promoting Bacillusweihenstephanensis isolated from serpentine soil in Portugal. J Basic Microbiol 48:500–508CrossRefGoogle Scholar
  70. Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149CrossRefGoogle Scholar
  71. Saleem M, Arshad M, Hussain S, Bhatti AS (2007) Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J Ind Microbiol Biotechnol 34:635–648CrossRefGoogle Scholar
  72. Sandip B, Subrata P, Swati RG (2011) Isolation and characterization of plant growth promoting Bacillus Thuringiensis from agricultural soil of West Bengal. Res J Biotech 6:9–13Google Scholar
  73. Schalk IJ, Hannauer M, Braud A (2011) New roles for bacterial siderophores in metal transport and tolerance. Environ Microbiol 13:2844–2854CrossRefGoogle Scholar
  74. Shaharoona B, Jamro GM, Zahir ZA, Arshad M, Memon KS (2007) Effectiveness of various Pseudomonas spp. and Burkholderia caryophylli containing ACC-deaminase for improving growth and yield of wheat (Triticumaestivum L.). J Microbiol Biotechnol 17:1300–1307Google Scholar
  75. Singh AK, Cameotra SS (2013) Rhamnolipids production by multi-metal-resistant and plant-growth-promoting rhizobacteria. Appl Biochem Biotechnol 170:1038–1056CrossRefGoogle Scholar
  76. Singh Y, Ramteke PW, Shukla PK (2013) Isolation and characterization of heavy metal resistant Pseudomonas spp. and their plant growth promoting activities. Adv Appl Sci Res 4:269–272Google Scholar
  77. Sun L, He L, Zhang Y, Zhang W, Wang Q, Sheng X (2009) Isolation and biodiversity of copper-resistant bacteria from rhizosphere soil of Elsholtziasplendens. Wei Sheng Wu Xue Bao 49:1360–1366Google Scholar
  78. Suresh B, Ravishankar GA (2004) Phytoremediation-a novel and promising approach for environmental clean-up. Crit Rev Biotechnol 24:97–124CrossRefGoogle Scholar
  79. Swain H, Abhijita S (2013) Nitrogen fixation and its improvement through genetic engineering. J Global Biosci 2:98–112Google Scholar
  80. Tank N, Saraf M (2009) Enhancement of plant growth and decontamination of nickel-spiked soil using PGPR. J Basic Microbiol 49:195–204CrossRefGoogle Scholar
  81. Upadhayay A, Srivastava S (2012) Evaluation of multiple plant growth promoting traits of an isolate of Pseudomonasfluorescens strain Psd. Indian J Exp Biol 48:601–609Google Scholar
  82. Walker TS, Bais HP, Deziel E, Schweizer HP, Rahme LG, Fall R, Vivanco JM (2004) Pseudomonas aeruginosa-plant root interactions. Pathogenicity, biofilm formation and root exudation. Plant Physiol 134:320–331CrossRefGoogle Scholar
  83. Wani PA, Khan MS (2010) Bacillus species enhance growth parameters of chickpea (Cicerarietinum L.) in chromium stressed soils. Food Chem Toxicol 48:3262–3267CrossRefGoogle Scholar
  84. Waterlot C, Bidar G, Pelfrêne A, Roussel H, Fourrier H, Douay F (2013) Contamination, fractionation and availability of metals in urban soils in the vicinity of former lead and zinc smelters, France. Pedosphere 23:143–159CrossRefGoogle Scholar
  85. Zahir ZA, Ghani U, Naveed M, Nadeem SM, Asghar HN (2009) Comparative effectiveness of Pseudomonas and Serratia sp. containing ACC-deaminase for improving growth and yield of wheat (Triticum aestivum L.) under salt-stressed conditions. Arch Microbiol 191:415–424CrossRefGoogle Scholar
  86. Zaidi S, Usmani S, Singh BR, Musarrat J (2006) Significance of Bacillus subtilis strain SJ 101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64:991–997CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Agricultural Microbiology, Faculty of Agricultural SciencesAligarh Muslim UniversityAligarhIndia

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