Role of soil rhizobacteria in phytoremediation of heavy metal contaminated soils

Role of soil rhizobacteria in phytoremediation of heavy metal contaminated soils 1 2 first-author †E-mail:jingyande@163.comzhe@mail.ifas.ufl.edu †E-mail:jingyande@163.comzhe@mail.ifas.ufl.edu jingyande@163.com 1 3 corresp ‡Corresponding Author ‡Corresponding Author †E-mail:jingyande@163.comzhe@mail.ifas.ufl.edu †E-mail:jingyande@163.comzhe@mail.ifas.ufl.edu jingyande@163.com 1 Ministry of Education Key Lab of Environment, Remediation and Ecosystem Health, School of Natural Resource and Environment Science, Zhejiang University, Hangzhou 310029, China Ministry of Education Key Lab of Environment, Remediation and Ecosystem Health, School of Natural Resource and Environment Science, Zhejiang University, Hangzhou 310029, China Department of Resources and Planning, Qufu Normal University, Jining 273165, China Department of Resources and Planning, Qufu Normal University, Jining 273165, China University of Florida Institute of Food and Agricultural Sciences, Indian River Research and Education Center, Fort Pierce, Florida 34945, USA University of Florida Institute of Food and Agricultural Sciences, Indian River Research and Education Center, Fort Pierce, Florida 34945, USA Heavy metal pollution of soil is a significant environmental problem and has its negative impact on human health and agriculture. Rhizosphere, as an important interface of soil and plant, plays a significant role in phytoremediation of contaminated soil by heavy metals, in which, microbial populations are known to affect heavy metal mobility and availability to the plant through release of chelating agents, acidification, phosphate solubilization and redox changes, and therefore, have potential to enhance phytoremediation processes. Phytoremediation strategies with appropriate heavy metal-adapted rhizobacteria have received more and more attention. This article paper reviews some recent advances in effect and significance of rhizobacteria in phytoremediation of heavy metal contaminated soils. There is also a need to improve our understanding of the mechanisms involved in the transfer and mobilization of heavy metals by rhizobacteria and to conduct research on the selection of microbial isolates from rhizosphere of plants growing on heavy metal contaminated soils for specific restoration programmes. Rhizobacteria Phytoremediation Heavy metals Rhizosphere INTRODUCTION 1 Soil pollution by heavy metals 2 Heavy metals are conventionally defined as elements with metallic properties (ductility, conductivity, stability as cations, ligand specificity, etc.) and an atomic number > 20. The most common heavy metal contaminants are Cd, Cr, Cu, Hg, Pb and Ni. Metals are natural components in soil with a number of heavy metals being required by plants as micronutrients. However, pollution of biosphere by toxic metals has accelerated dramatically since the beginning of the industrial revolution. As a result of human activities such as mining and smelting of metals, electroplating, gas exhaust, energy and fuel production, fertilizer, sewage and pesticide application, municipal waste generation, etc. (Kabata-Pendias and Pendias, 1989 1989 ), metal pollution has become one of the most severe environmental problems today. Excessive accumulation of heavy metals is toxic to most plants. Heavy metals ions, when present at an elevated level in the environment, are excessively absorbed by roots and translocated to shoot, leading to impaired metabolism and reduced growth (Bingham et al., 1986 1986 ; Foy et al., 1978 1978 ). Heavy metal contamination to water and soil poses a major environmental and human health problem. In addition, excessive metal concentrations in contaminated soils result in decreased soil microbial activity and soil fertility, and yield losses (McGrath et al., 1995 1995 ). Cadmium, as a non-essential, toxic heavy metal to plants, which may well demonstrate the problem, can inhibit root and shoot growth, affect nutrient uptake and homeostasis, and is frequently accumulated by agriculturally important crops (Sanità di Toppi and Gabrielli, 1999 1999 ). Thus, when Cd-enriched crop products are consumed by animals and humans, it can cause diseases. On condition that soil Cd pollution is cumulative with levels increasing over time, the soil may eventually become unusable for crop production. Similarly, contamination of soil with Cd can negatively affect biodiversity and the activity of soil microbial communities (McGrath, 1994 1994 ). Burd et al.( 1998 1998 )’s experiments revealed that canola seeds developed normally in the presence of up to 1 mmol/L nickel chloride, but that plant root and shoot elongation were inhibited at higher levels. Remediation technologies 2 Heavy metals cannot be destroyed biologically (no “degradation”, change in the nuclear structure of the element, occurs) but are only transformed from one oxidation state or organic complex to another (Garbisu and Alkorta, 2001 2001 ), remediation of heavy metal contamination in soils is more difficult. Until now, methods used for their remediation such as excavation and land fill, thermal treatment, acid leaching and electroreclamation are not suitable for practical applications, because of their high cost, low efficiency, large destruction of soil structure and fertility and high dependence on the contaminants of concern, soil properties, site conditions, and so on. Thus, the development of phytoremediation strategies for heavy metals contaminated soils is necessary (Chaney et al., 2000 2000 ; Cheng et al., 2002 2002 ; Lasat, 2002 2002 ). Phytoremediation assisted by soil rhizobacteria 2 Phytoremediation, the use of plants to extract, sequester, and/or detoxify pollutants through physical, chemical, and biological processes (Cunningham and Ow, 1996 1996 ; Saxena et al., 1999 1999 ; Wenzel et al., 1999 1999 ), has been reported to be an effective, in situ, non-intrusive, low-cost, aesthetically pleasing, ecologically benign, socially accepted technology to remediate polluted soils (Alkorta and Garbisu, 2001 2001 ; Garbisu et al., 2002 2002 ; Weber et al., 2001 2001 ). It also helps prevent landscape destruction and enhances activity and diversity of soil microorganisms to maintain healthy ecosystems, which is consequently considered to be a more attractive alternative than traditional methods to the approaches that are currently in use for dealing with heavy metal contamination (Bogardt and Hemmingsen, 1992 1992 ; Cunningham and Berti, 1993 1993 ; Cunningham and Ow, 1996 1996 ; Cunningham et al., 1995 1995 ; Salt et al., 1995 1995 ). Fig. 1 1 plots the process of metal uptake and accumulation in plants. 1: A metal iron is sorbed at root surface; 2: Bioavailable metal moves across cellular membrane into root cells; 3: A fraction of the metal absorbed into roots is immobilized in the vacuole; 4: Intracellular mobile metal crosses cellular membranes into root vascular tissue (xylem); 5: Metal is translocated from the root to aerial tissues (stems and leaves) Phytoremediation of heavy metals may take one of several forms: phytoextraction, rhizofiltration, phytostabilization, and phytovolatilization. Phytoextraction refers to processes in which plants are used to concentrate metals from the soil into the roots and shoots of the plant; rhizofiltration is the use of plant roots to absorb, concentrate or precipitate metals from effluents; and phytostabilization is the use of plants to reduce the mobility of heavy metals through absorption and precipitation by plants, thus reducing their bioavailability; phytovolatilization is the uptake and release into the atmosphere of volatile materials such as mercury- or arsenic-containing compounds. The ideal plant for phytoextraction should grow rapidly, produce a high amount of biomass, and be able to tolerate and accumulate high concentrations of metals in shoots. Most of the commonly known heavy metal accumulators belong to the Brassicaceae family (Kumar et al., 1995 1995 ). Although hyperaccumulator plants have exceptionally high metal accumulating capacity, most of these have a slow growth rate and often produce limited amounts of biomass when the concentration of available metal in the contaminated soil is very high. An alternative is to use species with a lower metal accumulating capacity but higher growth rates, such as Indian mustard ( Brassica juncea ); another alternative is to provide them with an associated plant growth-promoting rhizobacteria, which also is considered to be an important component of phytoremediation technology (Wenzel et al., 1999 1999 ; Glick, 2003 2003 ). Obviously, the rhizosphere contains a large microbial population with high metabolic activity compared to bulk soil (Anderson et al., 1993 1993 ). Microbial populations are known to affect heavy metals mobility and availability to the plant through release of chelating agents, acidification, phosphate solubilization, and redox changes (Abou-Shanab et al., 2003a 2003a ; Smith and Read, 1997 1997 ). Especially, some plant growth-promoting bacteria associated with plant roots also may exert some beneficial effects on plant growth and nutrition through a number of mechanisms such as N 2 fixation, production of phytohormones and siderophores, and transformation of nutrient elements when they are either applied to seeds or incorporated into the soil (Kloepper et al., 1989 1989 ; Glick, 1995 1995 ; Glick et al., 1999 1999 ). The use of rhizobacteria in combination with plants is expected to provide high efficiency for phytoremediation (Abou-Shanab et al., 2003a 2003a ; Whiting et al., 2001 2001 ). Therefore, the potential and the exact mechanism of rhizobacteria to enhance phytoremediation of soil heavy metals pollution have recently received some attention (de Souza et al., 1999a 1999a ; Whiting et al., 2001 2001 ). For example, Burd et al.( 1998 1998 ) observed that both the number of Indian mustard seeds that germinated in a nickel-contaminated soil, and the attainable plant size increased by 50%~100% by the addition of K . ascorbata SUD165/26, an associated plant growth-promoting rhizobacteria, to the soil in preliminary field trials, and de Souza et al.( 1999b 1999b ) investigated phytoremediation of Se and Hg in constructed wetlands and found that accumulation of Se and Hg were enhanced by rhziobacteria in wetland plant tissues. INTERACTIONS IN RHIZOSPHERE 1 Potential for phytoremediation depends upon the interactions among soil, heavy metals, bacteria, and plants. As shown schematically in Fig. 2 2 , these complex interactions are affected by a variety of factors, such as characteristics and activity of plant and rhizobateria, climatic conditions, soil properties, etc. Plant-bacteria interactions 2 The roots of plants interact with a large number of different microorganisms, with these interactions being major determinants of the extent of phytoremediation (Glick, 1995 1995 ). The functioning of associative plant-bacterial symbioses in heavy-metal-polluted soil can be affected from the side of both the micropartner (plant-associated bacteria) and the host plant. Soil microbes play significant roles in recycling of plant nutrients, maintenance of soil structure, detoxification of noxious chemicals, and control of plant pests and plant growth (Elsgaard et al., 2001 2001 ; Filip, 2002 2002 ; Giller et al., 1998 1998 ). Thus, bacteria can augment the remediation capacity of plants or reduce the phytotoxicity of the contaminated soil. In addition, plants and bacteria can form specific associations in which the plant provides the bacteria with a specific carbon source that induces the bacteria to reduce the phytotoxicity of the contaminated soil. Alternatively, plants and bacteria can form nonspecific associations in which normal plant processes stimulate the microbial community, which in the course of normal metabolic activity degrades contaminants in soil. Plants roots can provide root exudate, as well as increase ion solubility. These biochemical mechanisms increase the remediation activity of bacteria associated with plant roots. To sum up, the adaptation capabilities of both partners of the associative symbiosis as well as the bioremediation potential of the microsymbiont are of importance in minimizing the detrimental effect of heavy-metal pollution. Heavy metal-bacteria interactions 2 Rhizobacteria have been shown to possess several traits that can alter heavy metals bioavailability (Lasat, 2002 2002 ; McGrath et al., 2001 2001 ; Whiting et al., 2001 2001 ) through the release of chelating substances, acidification of the microenvironment, and by influencing changes in redox potential (Smith and Read, 1997 1997 ). For example, Abou-Shanab et al.( 2003a 2003a ) reported that the addition of Sphingomonas macrogoltabidus , Microbacterium liquefaciens , and Microbacterium arabinogalactanolyticum to Alyssum murale grown in serpentine soil significantly increased the plant uptake of Ni when compared with the un-inoculated controls as a result of soil pH reduction. However, heavy metals are known to be toxic to plants and most organisms when present in soils in excessive concentrations. Giller et al.( 1998 1998 ) reported that there was a detrimental effect to soil microbial diversity and microbial activities (indexes of microbial metabolism and of soil fertility) in metal-polluted environments. Plant-bacteria-soil interactions 2 The specificity of the plant-bacteria interaction is dependent upon soil conditions, which can alter contaminant bioavailability, root exudate composition, and nutrient levels. In addition, the metabolic requirements for heavy metals remediation may also dictate the form of the plant-bacteria interaction i.e., specific or nonspecific. Along with metal toxicity, there are often additional factors that limit plant growth in contaminated soils including arid conditions, lack of soil structure, low water supply and nutrient deficiency. EFFECT OF RHIZOBACTERIA ON PHYTOREMEDIATION 1 Plant-growth 2 Rhizosphere microorganisms, which are closely associated with roots, have been termed plant growth promoting rhizobacteria (PGPR) (Glick, 1995 1995 ). Plant growth-promoting rhizobacteria include a diverse group of free-living soil bacteria that can improve host plant growth and development in heavy metal contaminated soils by mitigating toxic effects of heavy metals on the plants (Belimov et al., 2004 2004 ). Table 1 1 shows effects of variations of PGPR on plant. It is well known that heavy metals can even be toxic for metal-accumulating and metal-tolerant plants, if the concentration of metals in the environment is sufficiently high. This is partly attributable to iron deficiency in a range of different plant species (Mishra and Kar, 1974 1974 ; Ma and Nomoto, 1993 1993 ; Römheld and Marschner, 1986 1986 ; Wallace et al., 1992 1992 ) in heavy metal contamination soil. Furthermore, the low iron content of plants that are grown in the presence of high levels of heavy metals generally results in these plants becoming chlorotic, since iron deficiency inhibits both chloroplast development and chlorophyll biosynthesis (Imsande, 1998 1998 ). However, microbial iron-siderophore complexes can be taken up by plants, and thereby serve as an iron source for plants (Bar-Ness et al., 1991 1991 ; Reid et al., 1986 1986 ; Wang et al., 1993 1993 ). It was therefore reasoned that the best way to prevent plants from becoming chlorotic in the presence of high levels of heavy metals was to provide them with an associated siderophore-producing bacterium. This suggests that some plant growth-promoting bacteria can significantly increase the growth of plants in the presence of heavy metals including nickel, lead and zinc (Burd et al., 1998 1998 ; 2000 2000 ), thus allowing plants to develop longer roots and get better established during early stages of growth (Glick et al., 1998 1998 ). Once the seedling is established, the bacterium can also help the plant acquire sufficient iron for optimal plant growth. Similarly, chromium-resistant pseudomonads, isolated from paint industry effluents, were able to stimulate seed germination and growth of Triticum aestivus in the presence of potassium bichromate (Hasnain and Sabri, 1996 1996 ). In this case, the bacterial enhancement of seedling growth was associated with reduced chromium uptake. The effect of adding K . ascorbata SUD165, a plant growth-promoting bacterium, to canola or tomato seeds before the seeds germinate, was also examined in the presence of inhibitory concentrations of Ni 2+ . The results of these experiments showed that at all concentrations of nickel tested (1 to 6 mmol/L Ni 2+ ), using both a low-level and a high-level bacterial cell treatment (cell suspension absorbance of 0.025 or 0.50, respectively), with both canola and tomato plants, with both roots and shoots, and in both pouches and pots, the addition of K . ascorbata SUD165 significantly decreased the toxicity of the added nickel (Burd et al., 1998 1998 ). PGPR Plant Effects References Delftia tsuruhatensis , strain HR4, Pseudomonas corrugata 13 or Pseudomonas aureofaciens 63±28 Rice, cucumber Suppressant to plant pathogens Han et al., 2005 2005 ; Kamnev et al., 2005 2005 Bacillus licheniformis CECT5106, B . pumilus CECT5105, Bacillus licheniformis , Serratia proteamaculans 1-102, Serratia liquefaciens 2-68, Pseudomonas sp. strain GRP3, Pseudomonas alcaligenes PsA15, P . denitrificans PsD6, Bacillus polymyxa BcP26, Mycobacterium phlei MbP18 Pinus pinea, European alder, corn, mung bean, cotton and pea Promotion of growth and nutrient uptake of plant Probanza et al., 2002 2002 ; Ramos et al., 2003 2003 ; Pan et al., 1999 1999 ; Sharma et al., 2003 2003 ; Egamberdiyeva and Höflich, 2004 2004 Kluyvera ascorbata SUD165 and SUD165/26, Pseudomonas tolaasii RP23 and Pseudomonas fluorescens RS9, Variovorax paradoxus , Rhodococcus sp. and Flavobacterium sp. Tomoto, canola, perennial grasses ( Graminaceae ), and Indian mustard ( Brassica juncea L. Czern.) Resistant to Cd, Zn, Cu, Ni, Co, Cr, Pb and stimulation to root elongation of plant seedlings Burd et al., 1998 1998 ; 2000 2000 ; Dell’Amico et al., 2005 2005 ; Belimov et al., 2005 2005 Achromobacter piechaudii ARV8 Tomatoes and peppers Resistant to water and salt stress Mayak et al., 2004a 2004a ; 2004b 2004b Bacteria in the rhizosphere are involved in the accumulation of potentially toxic trace elements into plant tissues. de Souza et al.( 1999b 1999b ) found that axenic saltmarsh bulrush plants supplied with different rhizosphere bacteria accumulated (70±80)% higher Se concentrations in their roots and (40±60)% higher Se concentrations in shoots than plants grown under axenic conditions. Four out of the six bacterial strains tested significantly enhanced Se accumulation in roots and shoots of axenic plants when they were added as pure cultures ( P < 0.05; n =3). A mixture of the six bacterial strains tested also enhanced Se accumulation in axenic bulrush plants. However, there were some opposite viewpoints that the presence of ectomycorrhizal or vesicular-arbuscular fungi on the roots of plants decreased the uptake of metals by the plants and thereby increased plant biomass (Bradley et al., 1982 1982 ; Brown and Wilkins, 1985 1985 ; Dueck et al., 1986 1986 ; Heggo et al., 1990 1990 ; Killham and Firestone, 1983 1983 ; Tam, 1995 1995 ). The reason might be that some plants involve the use of plant growth-promoting bacteria or mycorrhizal fungi to lessen the deleterious effects of heavy metals. Rhizospheric microorganism 2 The rhizobacteria of metal accumulating and hyperaccumulating plants and their role in the tolerance to and uptake of heavy metals by the plants have been studied. Research has also shown that many rhizobacteria are tolerant to heavy metals and play important roles in mobilization or immobilization of heavy metals (Gadd, 1990 1990 ). It is now well-clarified that the population of rhizobateria is several orders of magnitude greater than that in the bulk soil with the elevated levels of heavy metals in these soils have significant impacts on microorganism population size, community structure, and overall activity of the soil microbial communities. Experiments showed that the number of bacteria in the rhizosphere of D . fusca reached 1.0×10 7 CFU/g. This relatively low bacterial count can be attributed to the presence of heavy metals in high concentrations (39 mg Co/kg, 3 mg Cd/kg, 79 mg Ni/kg, 30 mg Cu/kg, 4834 mg Zn/kg, 123 mg Cr/kg and 114 mg Pb/kg dry soil) (Abou-Shanab et al., 2005 2005 ). Chaudri et al.( 1992 1992 ) also found that rhizobium populations were reduced at concentrations > 7 mg/kg soil in their Cd treatments. Field studies of metal contaminated soils have similarly demonstrated that elevated metal loadings can result in decreased microbial community size (Brookes and McGrath, 1984 1984 ; Chander and Brookes, 1991 1991 ; Jordan and LeChevalier, 1975 1975 ; Konopka et al., 1999 1999 ). Besides, the microorganism community structure of the rhizosphere population is important in the context of plant growth. This is largely attributed to the finding that microbial populations often establish some sort of positive cooperation with the host plant system. For example, soil pollution with heavy metals could lead to the appearance of heavy-metal resistant rhizobateria in the soil of industrial regions (Aleem et al., 2003 2003 ). It was revealed that a high proportion of metal resistant bacteria persist in the rhizosphere of the hyperaccumulators Thalaspi caerulescens (Delorme et al., 2001 2001 ) and Alyssum bertolonii (Mengoni et al., 2001 2001 ) or Alyssum murale (Abou-Shanab et al., 2003a 2003a ) grown in soil contaminated with Zn and Ni or Ni, respectively. The presence of rhizobacteria increased concentrations of Zn (Whiting et al., 2001 2001 ), Ni (Abou-Shanab et al., 2003b 2003b ) and Se (de Souza et al., 1999a 1999a ) in T . caerulescens , A . murale and B . juncea , respectively. Multiple metal-resistance (MMR) in bacteria seems to be the rule rather than the exception. Abou-Shanab et al.( 2005 2005 ) tested the patterns of tolerance of the heavy metals in the 107 rhizobacterial isolates at 1 mmol/L concentrations and found all the rhizobacterial strains to be tolerant to multiple metal ions. Strains with hexa-, penta-, tetra-, and tri-metal ions tolerant, respectively, were found more frequent than those with hepta-, double and mono-tolerance. Notably cadmium, copper, lead, and nickel resistance seemed to be restricted to those strains which were resistant to six metals or more. Similar observations have been previously reported by Sabry et al.( 1997 1997 ). High levels of heavy metals could decrease rhizobateria metabolic activity, biomass and diversity (Gremion et al., 2004 2004 ; Sandaa et al., 1999 1999 ). The activities of the large population of bacteria inhabiting the rhizosphere can also be expected to influence heavy metals uptake by plants. It is reported that under non-sterile soil system, plants showed no iron-deficiency symptoms and have fairly high iron level in roots in contrast to plants grown in sterile system. This can attribute to rhizospheric microbial activity, which plays an important role in iron acquisition (Masalha et al., 2000 2000 ). Some rhizobateria can exude a class of rhizobateria secretion, such as antibiotics (including the antifungals), phosphate solubilization, hydrocyanic acid, indoleacetic acid (IAA), siderophores, 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase which increase bioavailability and facilitate root absorption of heavy metals, such as Fe (Crowley et al., 1991 1991 ) and Mn (Barber and Lee, 1974 1974 ), as well as nonessential metals, such as Cd (Salt et al., 1995 1995 ), enhance tolerance of host plants by improving the P absorption (Davies et al., 2001 2001 ; Liu et al., 2000 2000 ) and promote plant growth (Budzikiewicz, 1997 1997 ; Duffy and Défago, 1999 1999 ; Burd et al., 2000 2000 ; Ellis et al., 2000 2000 ; Meyer, 2000 2000 ). Abou-Shanab et al.( 2005 2005 ) investigated the correlation between metal resistance and metal mobilization abilities of rhizobacteria under heavy metals stress. The highest incidence of the biochemical activity of isolates and metal resistance was recorded for: phosphate solubilizers with Cr, Zn and Pb (92.5%, 82.2% and 68.2%), respectively; then for siderophore producers with Cr, Zn and Pb (78.5%, 71.02% and 61.6%), respectively, and finally for acid producers with Cr, Zn and Pb (63.5%, 53.3% and 42.9%), respectively. This implies that phosphate solubilization is not only the mechanism adopted by bacteria towards metals in soil; but that siderophores and acid production are involved in mobilizing metals. It should be mentioned that IAA production by rhizobacteria is believed to play an important role in plant-bacterial interactions (Lambrecht et al., 2000 2000 ). Therefore, any direct influence on IAA production by bacteria may in turn affect their phytostimulating efficiency. It has been well documented that the biosynthesis of auxins with their excretion into soil makes a major contribution to the bacterial plant-growth-promoting effect (Lambrecht et al., 2000 2000 ; Kamnev, 2003 2003 ; Steenhoudt and Vanderleyden, 2000 2000 ). It has been found that Cu 2+ and Cd 2+ significantly suppressed the production of IAA (auxin) by non-endophytic and facultatively endophytic strains of A . brasilense (Sp7 and Sp245, respectively), which can directly affect the plant-growth-stimulating efficiency of associative plant-bacterial symbioses in heavy-metal-polluted soils (Kamnev et al., 2005 2005 ). Kamnev et al.( 2005 2005 ) similarly discovered that both Cu 2+ and Cd 2+ ions significantly decreased the level of IAA production for strain Sp7, whereas the bacterial growth rate was virtually not affected. In addition, some plant growth-promoting bacteria i.e., free-living soil bacteria that are involved in a beneficial association with plants, contain the enzyme ACC deaminase (Glick, 1995 1995 ; Glick et al., 1995 1995 ; Jacobson et al., 1994 1994 ), which can cleave the plant ethylene precursor ACC and lower the level of ethylene in a developing or stressed plant. Plant growth-promoting bacteria that contain ACC deaminase may act to insure that the ethylene level does not impair root growth (Glick et al., 1998 1998 ), and that by facilitating the formation of longer roots, these bacteria may enhance seedling survival and plant root growth. Other properties of this bacterial strain, in addition to ACC deaminase activity, may contribute to this result: various N 2 -fixing and auxin-producing PGPR, siderophores, and antibiotics, all of which may stimulate plant growth in the presence of toxic metals concentrations. For example, Masalha et al.( 2000 2000 ) reported that plants grown under non-sterile soil systems were better in terms of iron nutrition to those grown under sterile condition. Their data emphasize the role of microbial community on the iron nutrition of plants. In fact, there is evidence that at least part of the toxic effects of some heavy metals in plants results from an induced iron deficiency, and since bacterial siderophores can provide iron to various plants (Bar-Ness et al., 1991 1991 ; Reid et al., 1986 1986 ; Wang et al., 1993 1993 ), siderophores produced by rhizobacteria may reduce nickel toxicity by supplying the plant with iron and hence reducing the severity of nickel toxicity (Bingham et al., 1986 1986 ; Bollard, 1983 1983 ; Foy et al., 1978 1978 ; Yang et al., 1996 1996 ). Bioavailability of toxic heavy metals 2 Soil rhizobateria can also directly influence metal solubility by changing heavy metal speciation in the rhizosphere. Study of the roles of mycorrhiza in metal speciation in the rhizosphere and the impact on increasing host plant tolerance against excessive heavy metals in soil showed that speciations of Cu, Zn and Pb changed significantly in the rhizosphere of AM (arbuscular mycorrhiza) infected and non-infected maize in comparison to bulk soil; The greatest change was exchangeable Cu that increased by 26% and 43% in non-infected and AM-infected rhizosphere, respectively, than in bulk soil. With the exception of organic bound Cu in AM, other speciations were stable in the rhizosphere of AM and non-AM treatments. It is understandable that Cu was activated by inducing rhizobacteria (Huang et al., 2005 2005 ). The organic bound Zn and Pb increased significantly in the rhizosphere in comparison to those in the bulked soil. In contrast, carbonate and Fe-Mn oxides of Zn and Pb did not exhibit significant changes. The results might indicate that mycorrhiza could protect its host plants from the phytotoxicity of excessive copper, zinc and lead by changing the speciation from bioavailable to the non-bioavailable form. The fact that copper and zinc accumulation in the roots and shoots of mycorrhiza infected plants were significantly lower than those in the non-infected plants might also suggest that mycorrhiza efficiently restricted excessive copper and zinc absorptions into the host plants (Huang et al., 2005 2005 ). Soil properties 2 Evidence has been shown that the chemical conditions of the rhizosphere differ from those of the bulk soil, as a consequence of various processes that are induced by plant roots and/or by the rhizobacteria (Hinsinger, 2001 2001 ; Marschner, 1995 1995 ). Plant-bacteria interactions could stimulate the production of compounds that could alter soil chemical properties in rhziosphere and enhance heavy metals accumulation in plants. For example, Delorme et al.( 2001 2001 ) found that soil acidification in the rhizosphere of Thalaspi caerulescens facilitates metal ion uptake by increasing metal ion mobility around the roots. de Souza et al.( 1999b 1999b ) also reported that the accumulation of Hg increases when the pH of the culture solution is lowered and hypothesized that rhziobacteria of the plants reduced the pH in the rhizosphere, thereby increasing Hg uptake into plants. A further study of the influence of hydrogen and aluminum ions on the growth of the associative nitrogen-fixing and growth-promoting bacteria Azospirillum lipoferum 137, Arthrobacter mysorens 7, Agrobacterium radiobacter 10, and Flavobacterium sp. L30 showed that the response of plants to the inoculation strongly varied from positive to negative with the soil pH (Belimov et al., 1998 1998 ). In addition, Microorganisms can remove a number of metals from the environment by reducing them to a lower redox state (Lovley, 1995 1995 ). Many of the microorganisms that catalyze such reactions use the metals as terminal electron acceptors in anaerobic respiration. Such microorganisms, known as dissimilatory metal-reducing bacteria, are phylogenetically (Lonergan et al., 1996 1996 ) and physiologically (Lovley et al., 1997 1997 ) diverse; although, most share the ability to use Fe 3+ and S 0 as terminal electron acceptors (Lovley et al., 1997 1997 ). The microbial reduction of Cr 6+ to Cr 3+ has been one of the most widely studied forms of metal bioremediation (Lovley, 1995 1995 ; Wang and Shen, 1995 1995 ). A wide diversity of heterotrophic organisms are known to carry out this reaction which, depending upon the organism, can take place anaerobically or aerobically (Wang and Shen, 1995 1995 ; Lovley, 1993 1993 ). Plant pathogens 2 Plant growth-promoting bacterial could induce resistance in plants against fungal, bacterial and viral diseases (Maurhofer et al., 1998 1998 ), and insect (Zehnder et al., 1997 1997 ) and nematode pests (Sikora, 1992 1992 ). The induction of systemic resistance by rhizobacteria is referred to as ISR. In recent years, the use of PGPR as an inducer of systemic resistance in crop plants against different pathogens has been demonstrated under field conditions (Wei et al., 1991 1991 ; 1996 1996 ; Vidhyasekaran and Muthamilan, 1999 1999 ; Viswanathan and Samiyappan, 1999 1999 ). Nie et al.( 2002 2002 ) reported that antibiotic-secreting plant growth-promoting bacterial strains can inhibit the proliferation and subsequent invasion of phytopathogens, hence protecting plants from further damage in the presence of arsenate. Experiments showed that seed treated with P . fluorescens strain 97 protected beans against halo blight disease caused by Pseudomonas syringae pv. phaseolicola (Alstrom, 1991 1991 ). Reports on PGPR-mediated ISR against insects are restricted to very few crops. Induction of systemic resistance by PGPR strains, viz., P . putida strain 89B-27, S . marcescens strain 90-166, Flavomonas oryzihabitans strain INR-5 and Bacillus pumilus strain INR-7 have significantly reduced populations of the striped cucumber beetle, Acalyma vittatum and the spotted cucumber beetle, Diabrotica undecimpunctata howardi on cucumber (Zehnder et al., 1997 1997 ). PGPR also induces systemic resistance against nematode pests (Oostendorp and Sikora, 1990 1990 ; Sikora, 1992 1992 ; Sikora and Hoffmann-Hergarten, 1992 1992 ). P . fluorescens has induced systemic resistance and inhibited early root penetration of Heterodera schachtii , the cyst nematode in sugar beet (Oostendorp and Sikora, 1989 1989 ; 1990 1990 ). MECHANISMS OF RHZIOBACTERIA INFLUENCING HEAVY METAL ACCUMULATION 1 Rhizobacteria secretion 2 As mentioned above, rhziobacteria secretion may play a major role among mechanisms of phytoremediation assisted by rhziobacteria. Indirect mechanisms include preventing phytopathogens from inhibiting plant growth and development while direct mechanisms include: nitrogen fixation; synthesis of siderophores which can solubilize and sequester iron from the soil; production of phytohormones such as auxins and cytokinins, which can enhance plant growth; and solubilization of minerals such as phosphorus (Kloepper et al., 1989 1989 ; Glick, 1995 1995 ; Glick et al., 1999 1999 ; Patten and Glick, 1996 1996 ). Rhizobacteria produce metal-chelating agents called siderophores, which have an important role in the acquisition of several heavy metals (Leong, 1986 1986 ). These organic substances have the effect of scavenging Fe 3+ and significantly enhancing the bioavailability of soil bound iron (Kanazawa et al., 1994 1994 ). It has also been recognized that plants grown in metal-contaminated soils are often iron deficient, the production of siderophores by plant growth-promoting bacteria may help plants obtain sufficient iron (Burd et al., 2000 2000 ; Wallace et al., 1992 1992 ). Microbial siderophores are used as iron chelating agents that can regulate the availability of iron in the plant rhizosphere (Bar-Ness et al., 1992 1992 ; Loper and Henkels, 1999 1999 ). It has been assumed that competition for iron in the rhizosphere is controlled by the affinity of the siderophore for iron and ultimately decides the rhizosphere population structure. The important factors, which participate, are concentration of various types of siderophore, kinetics of exchange, and availability of Fe-complexes to microbes as well as plants (Loper and Henkels, 1999 1999 ). Interestingly, the binding affinity of phytosiderophores for iron is less than the affinity of microbial siderophores, but plants require a lower iron concentration for normal growth than do microbes (Meyer, 2000 2000 ). A number of PGPR, which stimulate root growth of different plant species including Indian mustard (Burd et al., 1998 1998 ; Belimov et al., 2001 2001 ), contain the enzyme ACC deaminase, which hydrolyses and decreases the amount of ACC, an ethylene precursor of the plant hormone ethylene, in plants and, as a result, to decrease ethylene biosynthesis by plants (Glick et al., 1994 1994 ; 1998 1998 ; Hall et al., 1996 1996 ). The model which represents how a PGPR bound to either a seed or plant root lowers the ethylene concentration and thereby prevents ethylene inhibition of root elongation was previously proposed by Glick et al.( 1998 1998 ). In some of the plants, ACC is exuded from roots or seeds and then taken up by the bacterium and cleaved by ACC deaminase to ammonia and α-ketobutyrate (Glick et al., 1998 1998 ). The bacteria utilize the ammonia evolved from ACC as a nitrogen source and thereby decrease ACC within the plant (Penrose and Glick, 2001 2001 ) with the concomitant reduction of plant ethylene and promoting root elongation (Burd et al., 1998 1998 ; Mayak et al., 1999 1999 ; Grichko and Glick, 2001 2001 ; Belimov et al., 2002 2002 ). To maintain the gradient between internal and external ACC levels, the plant must exude increasing amounts of ACC. The lowering of ACC levels within the plant results in a reduction in the amount of plant ethylene and a decreased extent of ethylene inhibition of plant seedling root elongation. This model may also be invoked to explain how plant growth-promoting bacteria lower the concentration of stress ethylene in plants. Evidence for this model includes the fact that the ability of a bacterium to promote root elongation is positively correlated with both the ACC deaminase activity of the bacterium and the ACC content (measured by high-pressure liquid chromatography) of the plant tissues. In addition, depending on the conditions, plant root growth may also be stimulated by IAA produced by PGPR bound to the seeds or roots (Patten and Glick, 2002 2002 ). As a matter of fact, low levels of IAA produced by rhizobacteria promote primary root elongation, whereas high levels of IAA stimulate lateral and adventitious root formation (Glick, 1995 1995 ) but inhibit primary root growth (Xie et al., 1996 1996 ). Thus, plant growth-promoting bacteria can facilitate plant growth by altering the hormonal balance within the affected plant (Glick et al., 1999 1999 ). Similarly, although an ethylene pulse is important in breaking seed dormancy, too much ethylene can inhibit plant seed germination (Bewley and Black, 1985 1985 ; Mayer and Poljakoff-Mayber, 1989 1989 ; Smalle and van der Straeten, 1997 1997 ). As just described above, a significant portion of the damage to plants from infection with fungal phytopathogens may occur as a direct result of the response of the plant to the increased level of stress ethylene (van Loon, 1984 1984 ). In the presence of fungal pathogens, not only does exogenous ethylene increase the severity of a fungal infection but also inhibitors of ethylene synthesis can significantly decrease the severity of infection. Since the enzyme ACC deaminase, when present in plant growth-promoting bacteria, can act to modulate the level of ethylene in a plant, lower the stress placed on plants by the presence of heavy metals and therefore ameliorate some of the apparent toxicity of heavy metals to plants. High surface area-to-volume ratio 2 Soil rhizobacteria, with activity and a high surface area-to-volume ratio because of their small size and therefore providing a large contact area, may have the potential to act as microbial chelates associated with phytoremediation (Anderson et al., 1993 1993 ; Kärenlampi et al., 2000 2000 ; Sitaula et al., 1999 1999 ). Indian mustard plants germinated on Se-containing media from axenic seeds coated with bacteria produced more root hairs and accumulated more Se than plants grown from axenic seeds (de Souza et al., 1999a 1999a ). However, increased root surface area caused by bacteria cannot solely account for the increased heavy metals accumulation, because bacteria were not involved in the accumulation of other heavy metals. Antibiotic experiments performed with bulrush and rabbitfoot grass supplied with chromate and arsenate showed no differences between Cr and As accumulation in antibiotic-supplied and untreated plants (de Souza et al., 1999b 1999b ). Transform toxic heavy metals 2 The efficiency of phytoremediation is also influenced by the bioavailability of metals to plants in soil. Bacteria may transform toxic heavy metals to forms that are more readily taken up into roots. For example, bacteria could enhance Se accumulation in plants by reducing selenate to organic Se, and organoselenium forms like SeMet are known to be taken up at faster rates into roots than inorganic forms (Zayed et al., 1998 1998 ). Huang et al.( 2005 2005 ) further depicts the relative changes as the percentages of the speciation concentration difference between bulked soil and rhizosphere to the concentration of bulked soil. Results showed that the relative changes of organic bound Cu, Zn and Pb were, respectively, +5%, +23%, +3% in the infected rhizosphere, and 0.8%, −3%, −2% in the noninfected rhizosphere. Thus, significant amounts of Cu, Zn and Pb were bounded by organic matter in the infected rhizosphere. Soil rhizobateria can also directly influence metal bioavailability by altering their chemical properties, such as pH, organic matter content, redox state, etc. This can aid in the leaching of these contaminants from soils. The bioavailability of heavy metals in soils is a function of its solubility (Ernst, 1996 1996 ) with pH and organic matter content being the main controlling factors (Gray et al., 1998 1998 ). For example, a strain of Pseudomonas maltophilia was shown to reduce the mobile and toxic Cr 6+ to nontoxic and immobile Cr 3+ , and also to minimize environmental mobility of other toxic ions such as Hg 2+ , Pb 2+ , and Cd 2+ (Blake et al., 1993 1993 ; Park et al., 1999 1999 ). Inhibition of plant pathogens 2 PGPR provides different mechanisms for suppressing plant pathogens. They include competition for nutrients and space (Elad and Baker, 1985 1985 ; Elad and Chet, 1987 1987 ), antibiosis by producing antibiotics viz., pyrrolnitrin, pyocyanine, 2,4-diacetyl phloroglucinol (Pierson and Thomashow, 1992 1992 ) and production of siderophores (fluorescent yellow green pigment), viz., pseudobactin which limits the availability of iron necessary for the growth of pathogens (Kloepper et al., 1980 1980 ; Lemanceau et al., 1992 1992 ). Other important mechanisms include production of lytic enzymes such as chitinases and β-1,3-glucanases which degrade chitin and glucan present in the cell wall of fungi (Fridlender et al., 1993 1993 ; Lim et al., 1991 1991 ; Potgieter and Alexander, 1996 1996 ; Velazhahan et al., 1999 1999 ), HCN production (Défago et al., 1990 1990 ) and degradation of toxin produced by pathogen (Borowitz et al., 1992 1992 ; Duffy and Défago, 1997 1997 ). Stimulation of transport protein 2 Bacterial survival and proliferation in the environment as well as within various hosts are critically dependent on the uptake and sequestration of transition metals such as manganese, zinc, and iron. For example, cells may stringently regulate intracellular zinc levels, since high concentrations of zinc are toxic to cellular functions and have evolved several types of proteins involved in binding and transport of zinc (Claverys, 2001 2001 ). Bacteria may also stimulate the sulfate transport protein, located in the root plasma membrane, which also transports selenate (Leggett and Epstein, 1956 1956 ). Inorganic Hg uptake in higher plants has not been well investigated, but has been linked to the passive uptake of lipophilic chloride complexes in phytoplankton (Mason et al., 1996 1996 ). CONCLUSION 1 When evaluating the effect of rhizobacteria on phytoremediation in contaminated soil, regardless of the precise effects used by the bacterium to protect plants, the results from literature suggest that certain bacteria may eventually find a use in the development of phytoremediation strategies. In this regard, heavy metals may be removed from polluted soil either by increasing the metal-accumulating ability of plants or by increasing the amount of plant biomass. In heavily contaminated soil where the metal content exceeds the limit of plant tolerance, it may be possible to treat plants with plant growth-promoting rhizobacteria, increasing plant biomass and thereby stabilizing, revegetating, and remediating metal-polluted soils. However, there are many areas of poor understanding or lack of information where more research is needed. They include: 1. Little has been done to investigate the microorganism induced changes in the rhizosphere of hyperaccumulator plants in relation to metal accumulation. Similarly, it is difficult to clarify specific features of microbial-plant and microorganism-soil interactions in the rhizosphere; 2. Further research is also needed to quantify the effect of rhizospheric processes induced by rhizobacteria on the phytoavailability of heavy metals; 3. Minimal work has been done to examine heavy metal speciation changes in the rhizosphere and to determine whether such changes could have altered the accumulation and distribution of heavy metals; 4. Rhizobacteria encounter soil solution before it enters the root and the sequestration of heavy metals by rhizobacteria from soil solution may play an important part in plant metals uptake. The role played by bacteria from soil solution in plant Cd uptake is still poorly understood; 5. 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Induction of systemic resistance in cucumber against cucumber beetles (Coleoptera: Chrysomelidae) by plant growth promoting rhizobacteria 10.1631/jzus.2007.B0192 Project supported by the National Natural Science Foundation of China (No. 20577044), the National Basic Research Program (973) of China (No. 2002CB410804), and the Program for Changjiang Scholars and Innovative Research Team in University (No. IRT0536), China 2006-03-16 2006-07-31 2022-01-05 Copyright © 2007, Journal of Zhejiang University Science 2007 Journal of Zhejiang University-SCIENCE B (Biomedicine and Biotechnology) 03 08