Author's personal copy · 2012. 9. 28. · Author's personal copy 172 L.E. de-Bashanet al. /...

Author's personal copy

Applied Soil Ecology 61 (2012) 171– 189

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Applied Soil Ecology

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The potential contribution of plant growth-promoting bacteria to reduceenvironmental degradation – A comprehensive evaluation

Luz E. de-Bashana,b, Juan-Pablo Hernandeza,b, Yoav Bashana,b,∗

a Environmental Microbiology Group, Northwestern Center for Biological Research (CIBNOR), Mar Bermejo 195, Col. Playa Palo de Santa Rita, La Paz, B.C.S. 23090, Mexicob The Bashan Foundation, 3740 NW Harrison Blvd., Corvallis, OR 97330, USA

a r t i c l e i n f o

Article history:Received 13 June 2011Received in revised form 19 August 2011Accepted 4 September 2011

This study is dedicated for the memory ofthe German/Spanish mycorrhizaeresearcher Dr. Horst Vierheilig(1960–2011) of CSIC, Spain.

Keywords:Desert reforestationMangrove restorationPhytoremediationPhytostabilizationRhizodegradationWater bioremediation

a b s t r a c t

Plant growth-promoting bacteria (PGPB) are commonly used to improve crop yields. In addition to theirproven usefulness in agriculture, they possess potential in solving environmental problems. Some exam-ples are highlighted. PGPB may prevent soil erosion in arid zones by improving growth of desert plantsin reforestation programs; in turn, this reduces dust pollution. PGPB supports restoration of mangroveecosystems that lead to improve fisheries. PGPB participate in phytoremediation techniques to decon-taminate soils and waters. These include: phytodegradation, phytotransformation, bioaugmentation,rhizodegradation, phytoextraction, phycoremediation, and phytostabilization, all leading to healthierenvironments. This review describes the state-of-the-art in these fields, examples from peer-reviewedliterature, pitfalls and potentials, and proposes open questions for future research.

© 2011 Elsevier B.V. All rights reserved.

1. Introduction

Plant growth-promoting bacteria (PGPB, Bashan and Holguin,1998; PGPR, Kloepper et al., 1980) are bacterial strains isolated fromdiverse environments with potential to positively influence manyparameters of plant growth and yield. As inoculants, single andcombinations of PGPB/PGPR are common and their use is increas-ing in agricultural practices (Díaz-Zorita and Fernández-Canigia,2009). PGPB affect plants through a multitude of mechanisms.Several comprehensive and critical reviews describing opera-tional mechanisms in PGPB/PGPR were published in recent years.It is likely that some mechanisms operating in crops are alsovalid for PGPB used in studies of environmental remediation(Bashan and de-Bashan, 2010; Lucy et al., 2004; Lugtenberg andKamilova, 2009). Consequently, general discussion of plausiblemechanisms for promoting plant growth will not be described inthis review.

∗ Corresponding autor at: Environmental Microbiology Group, Northwestern Cen-ter for Biological Research (CIBNOR), Mar Bermejo 195, Col. Playa Palo de Santa Rita,La Paz, B.C.S. 23090, Mexico. Tel.: +52 612 123 8484.

E-mail address: [email protected] (Y. Bashan).

There is a steady and serious decline in environmental healthworldwide and impairment of many ecosystems resulting fromhuman activities, some on a very large scale. These include defor-estation in the tropics and uncontrolled and unregulated releaseof pollutants to the environment. This indirectly increases expo-sure to environmental contaminants, heavy metals, and excessivenutrients (N and P) on a massive scale, impairing public healthin some countries. Traditional solutions for remediation, excava-tion and relocation of contaminants to landfills, are expensive andusually impractical because of the amount of soil involved, as inthe case of mine tailings. Additionally, new contaminated sitesof extensive size continue to increase. Consequently, more cost-effective remediation technologies are being investigated. One ofthe emerging strategies is the use of plants to extract, mitigate,and stabilize contaminants, which can be categorized as phytore-mediation and assist in reforestation (Cunningham et al., 1995;Ernst, 2005; Glick, 2003; Macek et al., 2000; McCutcheon andSchnoor, 2003; McGuinness and Dowling, 2009; Mench et al., 2006;Mukhopadhyay and Maiti, 2010; Pilon-Smits and Freeman, 2006;Weyens et al., 2009). As a strategy, and especially in comparison toremoval and relocation of contaminants, phytoremediation is inex-pensive. Benefits from successful approaches of phytoremediationinclude healthier soil, promoting and sustaining indigenous micro-bial communities that are essential for long-term bioremediation

0929-1393/$ – see front matter © 2011 Elsevier B.V. All rights reserved.doi:10.1016/j.apsoil.2011.09.003


172 L.E. de-Bashan et al. / Applied Soil Ecology 61 (2012) 171– 189

Fig. 1. Schematic representation of uses of plant growth-promoting bacteria and AM fungi in bioremediation processes.

of the soil, and creation of a more pleasing landscape, comparedwith ugly contaminated areas (Mendez and Maier, 2008). However,often the plants needed for phytoremediation cannot establish indegraded systems. Also, when established, they do not perform wellunder adverse environmental conditions, such as excessive con-centrations of contaminants, extreme high and low pH, deficientsupply of nutrients, poor or no soil structure, and severely dam-aged microbial communities. Under these conditions, inoculationof PGPB and sometimes AM fungi assist in phytoremediation. PGPBare experimentally employed to address environmental degrada-tion, such as revegetation and reforestation programs in areas oferoded soils, biological treatment of wastewater, phytoremedia-tion and phytostabilization of abandoned areas, and restoration ofmangroves (Bashan et al., 1999; de-Bashan et al., 2002a; Duponnoisand Plenchette, 2003; Grandlic et al., 2008; Hernandez et al., 2006;Kuiper et al., 2004; Lebeau et al., 2008; Ma et al., 2011; Stout andNüsslein, 2010; Sundararaman et al., 2007; Xue et al., 2009).

The aim of this review is to comprehensively describe the stateof the art in the use of PGPB in revegetation and reforestation ofareas undergoing desertification and contaminated sites, phytosta-bilization of mine tailings, phytoextraction of heavy metals andorganic contaminants, breakdown of contaminants using selectedplants, reforestation of mangroves, and enhancement of tertiarywastewater treatment (Fig. 1). Additionally, we present researchvenues likely to yield significant advances in knowledge to a levelof practical use of these emerging technologies.

2. Environmental applications of PGPB

2.1. PGPB for revegetation and reforestation of desertified lands

Soils in sub-humid, semi-arid, and arid areas are degraded byhuman activities (Wang et al., 2004) in a process called desertifica-tion. Desertification is an increasing major problem that reducesarable lands, increases soil erosion and flooding, reduces agri-cultural and forest production, reduces rural populations, andincreases respiratory health from dust pollution (McTainsh, 1986;Ortega-Rubio et al., 1998; Wang et al., 2004). Natural revegetation

in deforested deserts is either very slow, minimal, or does notoccur. These are common worldwide problems, which are par-ticularly severe in the Sahel of Africa and northeastern China. Inthe Americas, desertification is prevalent in the southwestern USA,northwestern Mexico, and arid regions of the Andes.

Desertified areas have hard-to-improve soil characteristics thatmake restoration difficult. By default, restoration of severelydegraded deserts with shrubs, trees, and cacti is always difficultand, in many cases, only marginally successful (Banerjee et al.,2006; Bean et al., 2004; Glenn et al., 2001; Roundy et al., 2001)due to several constrains. These constraints include: (1) the nursetree system governing natural vegetation is often destroyed andthe topsoil, with its beneficial microorganisms, are eroded by windand water, (2) organic matter is very low, soil structure is degraded,and (3) nutrients and water are usually in short supply. Whilethese limitations can be partly overcome by application of com-post, sludge from wastewater, and chemical fertilizers, these arecostly and impractical on a large scale. Consequently, natural suc-cession and revegetation in these arid zones, if it occurs, is veryslow. Establishing vegetation can be difficult, takes considerabletime, and are labor intensive. Any attempt to restore native plantsshould also consider restoring the beneficial microflora associatedwith trees and shrubs and provide organic matter (Bacilio et al.,2006; Grandlic et al., 2008; Velázquez-Rodríguez et al., 2001).

Various rehabilitation strategies have addressed restoration ofvegetation in desertified areas. These include reforestation withnative and exotic plants (Miyakawa, 1999; Moore and Russell,1990), urban, agricultural, and pastoral coverage (Portnov andSafriel, 2004), compost or sludge amendments to increase organicmatter and water-holding capacity (Mendez et al., 2007), and inoc-ulation with plant growth-promoting microorganism (Grandlicet al., 2008).

Reforestation of degraded lands undergoing erosion (Groverand Musick, 1990) involves at least three stages (Fig. 2). First, itis necessary to establish fast cover with native annuals to reduceerosion, a task difficult to achieve when rainfall is very low orunpredictable (Banerjee et al., 2006; Roundy et al., 2001). Second, acover with shrubs for short and medium term reforestation must be


L.E. de-Bashan et al. / Applied Soil Ecology 61 (2012) 171– 189 173

Fig. 2. Potential rehabilitation strategies to address desertification of eroded land.

established (Bean et al., 2004). Third, a long-term soil erosion pre-vention program, using long-lived and slow-growing trees, must beestablished; this includes tree-shaped cacti, such as the giant car-don cactus (Pachycereus pringlei) (Bashan et al., 1999, 2000b), theworld’s most massive cactus, and several other large and long-livedcacti and long-lived leguminous trees, such as mesquite (Drezner,2006).

One of the fundamental theories about the recurrent failure ofnatural revegetation in eroded desert areas and the difficulties toestablish planting or seeding native plants is that the topsoil has lostits beneficial plant-associated microorganisms and, consequently,part of its fertility and growth potential. Even during occasionalyears of plentiful rainfall, when establishment of desert plants ismore likely (Drezner, 2006), water alone does not substitute for theloss of soil fertility and microbial communities. At least some essen-tial plant growth-promoting microorganisms should be artificiallyreintroduced (Fig. 3).

PGPB and AM fungi are beneficial in harsh and limiting environ-ments because of their role in alleviating stress in plants (Sylviaand Williams, 1992). For example, PGPB of the genus Azospiril-lum exert their main growth-promoting effects when plants arestressed in saline soils (Bacilio et al., 2004), by drought (Creuset al., 1997, 1998), by excessive humic acids (Bacilio et al., 2003),under extreme pH (de-Bashan et al., 2005), and presence of heavymetals (Belimov and Dietz, 2000). Hyphae of AM fungi perme-ate large volumes of soil (Camel et al., 1991), interconnect rootsystems of adjacent plants, which facilitate exchange of nutrientsbetween them, and contribute to plant growth and soil structureas intimate associates with living cells within the roots and inthe soil (Bethlenfalvay and Schüepp, 1994; Bethlenfalvay et al.,2007; Wright and Upadhyaya, 1998). AM fungi are recognized asan essential component of plant–soil systems in deserts (Bashan

et al., 2000b, 2007; Bethlenfalvay et al., 1984; Carrillo-Garcia et al.,1999; Cui and Nobel, 1992; Nobel, 1996; Requena et al., 2001).PGPB do not yet have similar recognition and are used only at theexperimental level.

The use of PGPB for revegetation has several benefits: (1)reduces costs of bioremediation by decreasing the amount of fer-tilizer and compost; (2) allows establishment of plants in erodedzones where they had previously grown; and (3) improves planthealth and growth performance in eroded zones and enhances theirtolerance to drought and salinity.

Two strategies are used in the search for PGPB compatible witheroded zones. One is to isolate native PGPB from the soil or fromplants already growing there, propagate the PGPB, and use the PGPBas inoculants. This is a labor intensive procedure that has been suc-cessfully tried and explained below to remediate mine tailings. Theother approach examines isolates from the large number of avail-able and proven PGPB strains, mainly used in agriculture and usethem as inoculants in revegetation efforts.

Several studies, described in more detail later, document the useof the well-known PGPB Azospirillum brasilense of agricultural ori-gin for revegetation of degraded desert lands that have lost theircapacity to support regeneration. These areas remain barren fordecades (Bacilio et al., 2006; Bashan et al., 1999; Carrillo-Garciaet al., 2000). A. brasilense has proved to be an outstanding PGPBin hundreds of agricultural studies and was recently commercial-ized to use as an inoculant in crop cultivation (Díaz-Zorita andFernández-Canigia, 2009). It possesses multiple growth-promotingmechanisms: produces phytohormones (IAA, gibberellins, nitricoxide), has significant diazotrophic capacity, and participates inseveral small-magnitude mechanisms that work together or in tan-dem to enhance plant growth (Bashan and de-Bashan, 2010). Itplays a role in increasing acidification of inoculated rhizosphere



Fig. 3. Contributions and interactions of plant growth-promoting microorganisms and organic amendments during revegetation and reforestation of eroded soils.

of grains and cardon cactus that solubilize essential nutrients forplant growth that normally have extremely low bioavailability inalkaline desert soils (Carrillo et al., 2002).

Initial studies demonstrated that cells of A. brasilense inoculatedon giant cardon, the world’s largest cactus that stabilize topsoilin its usual desert scrub habitat, improve plant growth character-istics, are strain dependent, and are recoverable for at least 300days following inoculation (Puente and Bashan, 1993). This PGPBwas demonstrated in a field trial in Mexico, where three speciesof cacti had a significantly higher survival rate (76%), compared tonon-inoculated controls; <2% of the controls survived beyond 3.5years. Plants in this trial were inoculated three times each year for 2years; inoculation increased plant biomass and soil characteristicsin the experimental plots significantly improved. The most signifi-cant outcome from this trial was the great reduction in soil erosionand reclamation of topsoil (Bashan et al., 1999).

Growth chamber tests showed that A. brasilense enhancesenzymes in the phosphogluconate pathway and growth ofmesquite seedlings (Prosopis articulata) that is cultivated in poorsoils (Leyva and Bashan, 2008). Soil quality may play a role in theeffectiveness of inoculated PGPB. A. brasilense had no effect on thegrowth of the giant cardon cactus in rich soils found in desertresource islands. At the same time, root and above-ground growthof inoculated plants increased linearly after inoculation, enhancingdry shoot mass by 60% and root length by 100% in the poorest qual-ity soil (Carrillo-Garcia et al., 2000). Similarly, when A. brasilensewas used as an inoculant combined with compost in an attempt tomimic resource island soil, the outcome from inoculation was smallcompared to the effects of adding compost. Furthermore, PGPBtreatments were not significant at higher application rates of com-post (Bacilio et al., 2006). These studies emphasize the importanceof assessing soil quality before PGPB inoculations are assessed.

Under screenhouse cultivation common to these trees innurseries, three slow-growing leguminous trees used in desertreforestation and urban gardening in arid northwestern Mexicoand southwestern USA were measured to determine whethergrowth was promoted by inoculation with PGPB (A. brasilense andBacillus pumilus), unidentified arbuscular mycorrhizal (AM) fungi(mainly Glomus spp.), and a small supplement of common com-post. Mesquite (P. articulata) and yellow palo verde (Parkinsoniamicrophylla) had different, positive responses to several parame-ters, while blue palo verde (Parkinsonia florida) did not respond.After cultivation for 10 months, survival of the latter two species

was >80% and mesquite was almost 100%. Inoculation with growth-promoting microorganisms induce significant effects on the gasexchange of leaves of these trees, measured as transpiration and dif-fusion resistance, when these trees were cultivated without waterrestrictions (Bashan et al., 2009b).

In the field, using the same combination of inoculants as in thegreenhouse trials, seven field trials were undertaken with cardoncacti and three species of leguminous trees. The objective was toavoid the lengthy process of succession in deserts, usually requiredfor establishing climax-stage plants such as cardon. This normallyrequire establishment of cardon seedlings growing under legumi-nous nurse shrubs and trees, such as mesquite. Mesquite preventssoil erosion for several years or several decades, until cardon even-tually replace them and will stabilize the soil for centuries (Bashanet al., 1999, 2000b; Carrillo-Garcia et al., 1999; Solís-Domínguezet al., 2011; Stutz et al., 2000; Titus et al., 2003).

In these field experiments, association of cardon with any nurseshrub or tree increases survival and enhanced growth. For cardongrowing in isolation, compost, AM fungi, or combined treatmentsincreased survival. For cardon, no treatment influenced growthduring the first 3 months after transplanting. Later, all treatments,including PGPB, except for AM fungi, enhanced growth. However,2 years after transplanting to the field, enhanced growth by AMfungi was significant. This field study proposed that young legu-minous shrubs and trees enhance survival and growth of cardon,depending on the combination of leguminous nurse plant and cac-tus. Additional treatments, such as compost or PGPB, can eitheramplify or attenuate the effect (Bashan et al., 2009a). This studyalso demonstrated that in a reforestation program, nurse plantscan be very young. In nature, associations of young nurse plantswith cardon are uncommon; only plants >20 years have nurslings(Carrillo-Garcia et al., 1999).

This planting strategy (cardon-leguminous tree) may serve as ashortcut for establishing cardon seedlings in the field. In the earlyyears, nurse plants are much larger than young cardon, shade themand consequently make the water underneath their canopy moreavailable. Although additional treatments of compost and growth-promoting microorganisms are essential for survival and develop-ment of cardon growing without nurse trees, the effect of mesquiteon cardon development is more important over the long-termthan any microbial treatment provided when seedlings are planted.Furthermore, over time, even plants without inoculation of AMfungi become mycorrhizal because there are sufficient indigenous



AM fungi (Bashan et al., 2000b). The additional treatments had asynergistic effect only in the case of mesquite, the most commonnurse tree for cardon (Bashan et al., 2009b).

In other field experiments, survival of the three leguminoustrees (mesquite and two species of palo verde) was marginallyaffected by supplements after 30 months; survival was in the rangeof 60–90% of the trees, depending on the species, where all youngtrees survived >3 months under cultivation. Mesquite and yellowpalo verde responded (height, number of branches, and diameter ofthe main stem) positively to inoculation with PGPB, AM fungi, andcompost supplement, but blue palo verde did not respond to mosttreatments. Response, in terms of specific plant growth parame-ters to specific inoculations or amendments, depended mainly onthe tree species. This field study demonstrated that restoration ofseverely eroded desert lands is possible with native leguminoustrees supported with microbial agents and compost to increasesoil fertility and microbial activity near the trees (Bashan et al.,unpublished).

Taken together, application of all amendments in the field,as a single treatment, did not yield, as was initially assumed,synergistic or cumulative effects. Rather, the usefulness of eachamendment was mainly related to particular species, not as auniversal combination of amendments. Similarly to the desertrestoration, Quoreshi et al. (2008) demonstrates selective effects ofa microbial amendment when conifers and hardwoods in Canadawere inoculated with several mycorrhizae fungi at the nursery.Siviero et al. (2008) shows similar selective effects on the tropi-cal leguminous tree Schizolobium amazonicum, commonly used inagroforestry in the Amazon region, when inoculated with threearbuscular mycorrhizal fungi (Glomus clarum, Glomus intraradices,and Glomus etunicatum) associated with three strains of nitrogen-fixing bacteria, two Rhizobium spp. and one Burkholderia sp.

Another example from a desertified, semi-arid area of south-eastern Spain demonstrated that several exotic and native woodylegumes could be used in revegetation programs. Screening for theappropriate combination of plant and microsymbiont (mycorrhizaeand rhizobia) was previously tested. The results of a 4-year field trialshowed that only the native shrubby legumes were able to becomeestablished under local environmental conditions; hence, a specificreclamation strategy was recommended, which included inocula-tion with selected rhizobia and AM fungi for seedlings intended forrevegetation (Herrera et al., 1993). In a program of reforestationwith Pinus halepensis in degraded gypsiferous soil, two techniquescommonly used in restoring soil were compared: (1) inoculationwith selected strains of PGPB and (2) creation of a soil amendmentfrom urban waste. One year after planting, inoculation with twostrains of PGPB that had previously been used to enhance growthof Pinus spp. did not affect pine growth or the nutrient content ofneedles. However, significant increases in growth occurred underthe soil amendment treatment. Rincon et al. (2006) concluded thatscaling up greenhouse techniques, commonly used for PGPB ofleguminous trees, does not necessarily guarantee that other treespecies will receive the same benefits. In Korea, stimulation ofgrowth of wild plants using several species of PGPB was tested ona barren area; average shoot and root lengths and total dry weightof the plants grown in inoculated soil was far greater than plantsgrown in uninoculated soil (Ahn et al., 2007).

Other studies illustrate the value of using native PGPB. PGPBthat were obtained in an arid region improved rooting of mesquitecuttings (Felker et al., 2005). Cacti growing as pioneer plants onrock and cliffs devoid of soil materials provided strains of PGPBisolated from the surface of cardon roots (Puente et al., 2004a),endophytes of cardon (Puente et al., 2009a), and the surface of asmall cactus, Mammillaria fraileana (Lopez et al., 2011). These bac-teria weather the rock where the cacti grow, which release essentialminerals and produced small amounts of soil material that is later

washed down slopes and accumulate at lower elevations to sup-port desert plants that are not capable of pioneer growth on rock(Lopez et al., 2009). When endophytic bacteria are eliminated fromthe cacti seeds, seedlings grew more slowly. When sterilized seedswere inoculated with these bacteria and cultivated in pulverizedrock for 1 year, almost all of these bacteria enhanced plant growthin these harsh environments (Puente et al., 2004b, 2009b).

2.2. Revegetation with AM fungi and PGPB

In revegetation projects, using AM fungi alone or with PGPB iscommon in commercial reforestation of shrubs and trees in tem-perate areas (Chanway, 1997; Duponnois and Plenchette, 2003;Shishido et al., 1996), but far less in reforestation of deserts. Colo-nization by AM fungi of desert plants is found in numerous commontrees and cacti (Bashan et al., 2000b; Carrillo-Garcia et al., 1999)and relic trees (Bashan et al., 2007). Application of AM fungi is stilluncommon, although reforestation is now a priority in all Sahelianand Sudano-Sahelian countries, northern Mexico, and Australia. Itis likely that AM fungi play a similar role in desert plants as in agri-cultural crops growing in arid areas because plants rely on thesesymbiotic fungi to absorb nutrients, especially phosphorus andmineral transport in general. Yet, scientific data is in short supply.Many times, reforestation is done with fast-growing Acacia trees.The ability of Acacia to grow in low-nitrogen soils depends on theirability to form root symbiosis with both rhizobia and interactionwith AM fungi. Much of the nitrogen provided in the symbiosis isreturned to the soil through leaf fall; in turn, the humus improvesfertility and physical properties.

There are only a handful of examples of these multiple inocu-lations for restoring vegetation. (1) In semi-arid areas of southernEurope, a combination of AM fungi, rhizobia, and PGPB was used toenhance growth of the woody shrub Anthyllis cytisoides using native(Glomus coronatum) and exotic (G. intraradices) AM fungi. In reveg-etation programs, this shrub had greater root and shoot dry weightand enhanced root nodulation. PGPB also enhanced seedling ger-mination of this shrub. Native AM fungi were more effective thannon-native fungi species, indicating that native isolates are moresuitable to specific ecosystem conditions (Requena et al., 1997). (2)In a desertified ecosystem, specific combinations of AM fungi, PGPB,and Rhizobium spp. enhanced plant growth and uptake of nutri-ents. During a 5-year study, inoculation with AM fungi and rhizobiaenhanced establishment of key plant species, as well as increasedsoil fertility (Requena et al., 2001). (3) In southern Senegal, ectomy-corrhizal symbiosis of the strap wattle Acacia holosericea, a shrubfrom Australia, was directly promoted by 14 bacterial strains iso-lated from the soil mycorrhizosphere and the roots. Shoot mass wasenhanced by even more strains, all indicating the potential of somebacteria to help mycorrhiza in reforestation programs in the trop-ics (Founoune et al., 2002). (4) The bacterium Pseudomonas monteiliipromoted mycorrhiza colonization of A. holosericea of all species ofAcacia (Duponnois and Plenchette, 2003). (5) In a semi-arid area inSouthern Europe, a genetically modified bacterium performed lesswell to help mycorrhiza than wild strains (Valdenegro et al., 2001).(6) In tropical Southeast Asia, forest product companies used plantfast-growing and non-indigenous tree species to reduce regionalshortages of wood by cultivating black wattle or mangium, Acaciamangium, which grows rapidly on infertile soils and produces abun-dant wood in short rotations. Symbiosis between A. mangium andrhizobia and AM fungi is a management strategy where soils limitplant growth. Black wattle seedlings are sometimes inoculated withrhizobia and AM fungi in the nursery during early stages of growth.Aeroponics was used to produce saplings associated with AM fungithat were successfully transferred to the field (Martin-Laurent et al.,1999a,b).



In conclusion, there is no doubt that associative PGPB, rhizo-bia, and AM fungi can be successfully used in revegetation andreforestation programs. Applications should consider inherent lim-itations of PGPB, which work best on seedlings during initial stagesof growth, and using rhizobia and AM fungi that establish long-lasting associations with trees and shrubs in these programs. Sofar, no general interaction between a PGPB and a number of plantspecies was established on a long-term basis in the field, althoughsome beneficial associations were demonstrated under controlledconditions. Although there are experimental indications that inoc-ulation of a consortium of species might function better, it is notthe norm. Each combination of plant species, PGPB, and AM fungishould be tested separately before attempting large-scale revege-tation programs. This fact limits quick application of this promisingtechnology.

Mainly because of scarcity of studies on this topic, there arenumerous open questions; some have answers only in agriculturalstudies. Questions include: (1) are mycorrhizae-helping bacteriauseful in revegetation of eroded lands? (2) How do the PGPBenhance AM fungi infection in plants in the environment? (3) Arethe responses of AM fungi to PGPB similar to those of ectomyccor-rhiza to PGPB? (4) Because triple partnerships (plant–PGPB–AMfungi) and quadruple partnerships (when rhizobia are used inlegumes) produce a multiple of unpredicted interactions and pos-sibly complex mechanisms of action, would it be better to use onlyone type of microorganism? (5) Is it necessary to inoculate AM fungiwhen the soil has enough AM inoculum-potential, allowing inocu-lation with only PGPB to suffice? (6) Because inoculation of bacterialconsortia has not proven to be optimal in some cases, why does theenvironmental restoration industry use consortia as recommendedinoculants?

2.3. PGPB for restoration and reforestation mangrove ecosystems

Mangrove forests are vital tropical marine coastal ecosystemsfound at the intertidal zones of estuaries, backwaters, deltas, creeks,lagoons, marshes, and mud flats in tropical and subtropical regions(Spalding et al., 2010). Worldwide, mangroves are continually cutfor coastal urban development and aquaculture facilities; sincethe 1980s, over 25% of mangroves have been removed (Adeel andPomeroy, 2002; FAO, 2003; Rönnbäck, 1999). Mangroves providean essential environmental service, acting as safe havens and breed-ing grounds for countless marine species and waterfowl and arean irreplaceable prerequisite for coastal fisheries in the tropics(Holguin et al., 2001). Mangroves create a critical barrier that pro-tects coastal settlements and rice fields from tropical storms andtsunamis, mainly in Eastern Asia. Although mangroves in the wettropics are easy to reforest (Primavera et al., 2004), mangroves inarid and semi-arid regions are especially sensitive and have dif-ficulty regenerating after disruption (Toledo et al., 2001; Vovideset al., 2011a). The highly productive and diverse microbial com-munities living in mangrove ecosystems continuously transformnutrients from dead mangrove vegetation into sources of nitro-gen, phosphorus, and other mineral nutrients that are used bythe plants. In turn, exudates of plant roots serve as a food sourcefor the microbes and organisms higher up the food chain (Banoet al., 1997; Kathiresan and Bingham, 2001; Sahoo and Dhal, 2009).Holguin et al. (2001) predicted that, without restoring the micro-bial food web, restoration of mangroves would be very difficult,if not impossible. Efforts are currently underway to characterizethese ecosystems, including their microbial communities and themicrobial processes, with goals of developing successful restora-tion strategies. A secondary goal is to find microbial inoculantsthat can be used in agriculture in saline soils (Holguin et al., 2006;Sundararaman et al., 2007). These microbial communities includenitrogen-fixing bacteria and nitrogen cycle process (Flores-Mireles

et al., 2007; Hoffmann, 1999; Holguin et al., 1992; Sengupta andChaudhuri, 1990; Toledo et al., 1995a; Vovides et al., 2011a,b),phosphate-solubilizing bacteria (Rojas et al., 2001; Vazquez et al.,2000), methane generating bacteria (Giani et al., 1996; Mobanrajuet al., 1997; Strangmann et al., 2008), sulfate-reducing bacteria(Lokabharatbi et al., 1991; Sherman et al., 1998), and general het-erotrophic populations (Bano et al., 1997; Gonzalez-Acosta et al.,2006).

Bashan and Holguin (2002) initially proposed the use of PGPBfor reforestation of impaired mangroves and outlined the pos-sible microbial interactions in this process. They identified acollection of isolates that possessed beneficial growth-promotingtraits, including nitrogen fixation, phosphate solubilization, andphytohormone production (Fig. 4). Work applying PGPB to man-grove plants revealed that inoculation with the diazotrophiccyanobacterium Microcoleus chthonoplastes, isolated from aerialroots (pneumatophores) of mangroves, increased root colonizationof this bacterium on black mangroves and nitrogen accumulationin planta (Bashan et al., 1998; Toledo et al., 1995b). This cyanobac-terium and several other PGPB from mangroves have a beneficialside effect when introduced to dwarf saltwort Salicornia bigelovii,a halophytic annual that inhabits coastal marshes as well as man-groves. Inoculation enhanced plant biomass by 70% and improvesthe quality of the essential oils in this saltwort (Bashan et al., 2000a;Rueda-Puente et al., 2003).

Introducing the agricultural PGPB A. brasilense to mangroveseedlings demonstrated that two species, A. brasilense and Azospir-illum halopraeferens, have the ability to colonize root surfacesof black mangrove seedlings. A. halopraeferens was a better col-onizer and its presence on root surfaces was confirmed byscanning electron microscopy (Puente et al., 1999). Additionallaboratory and greenhouse studies use screening methods thatisolate and characterize large collections of potential PGPB (dia-zotrophs, denitrifying bacteria, phosphate-solubilizing bacteria)from mangroves and the conditions that control proliferation andinteraction among different species of bacteria (Flores-Mireleset al., 2007; Holguin and Bashan, 1996; Holguin et al., 2001;Rojas et al., 2001; Vazquez et al., 2000). For example, Kathiresanand Masilamani Selvam (2006) screened 48 isolates from man-groves and reported that two isolates demonstrated potential toincrease plant growth by >100%; hence, they are excellent can-didates for reforestation projects. El-Tarabily and Youssef (2010)studied an efficient phosphate-solubilizing bacterium, Oceanobacil-lus picturae, isolated from the rhizosphere of the gray mangroveAvicennia marina. In the greenhouse, inoculation of O. picturaeinto sediments amended with rock phosphate led to growth ofroots and shoots of seedlings that were significantly better thanseedlings in sediment amended only with rock phosphate. This bac-terium significantly increased available phosphate in the sediment,decreased the pH of the sediment, positively enhanced nutrientuptake parameters in roots and shoots, enhanced morphologicalparameters of the plants, and increased photosynthesis, comparedto plants grown in the identical sediment but without the bac-terium. Similarly, several Azotobacter species (A. chroococcum, A.virelandii, and A. beijerinckii) inoculated on red mangrove seedlings(Rhizophora) significantly increased average root biomass, rootlength, leaf area, shoot biomass, and concentrations of chloro-phylls and carotenoids, compared to controls (Ravikumar et al.,2004). Inoculation of black mangroves with undefined phosphatesolubilizers and nitrogen fixers improved growth of mangroveseedlings in nurseries (Galindo et al., 2006).

In summary, recent work with PGPB shows that mangroverhizosphere bacteria can be used to enhance reforestation withmangrove seedlings. This can be done by inoculating seedlingswith PGPB that participate in one or more of the microbial cyclesof the ecosystem. Still, the current state of knowledge on the



Fig. 4. Documented and proposed groups of bacteria and pathways that occur in mangrove ecosystems and have potential as a source for plant growth-promoting bacteriain mangroves and microbial sustenance of the mangrove ecosystem. This is a revision of the model originally proposed by Holguin et al. (2001) and Bashan and Holguin(2002).



microbiology of mangrove ecosystems leaves some fundamentalquestions unanswered. (1) Does nitrogen fixation and phosphatesolubilization in the ecosystem significantly contribute to the vital-ity of the trees? (2) Do mangrove specific PGPB exist or arethese strains common marine bacteria with PGPB traits? (3) Isit possible to enhance mangrove plant growth with terrestrial,agriculture-originated salt-tolerant PGPB? (4) Should restora-tion of conditions for microbial activity precede reforestation orare these processes interlinked? (5) Are techniques for inocula-tion with PGPB of terrestrial plants also applicable to wetlandplants?

2.4. PGPB for enhancing phytoremediation of contaminated soils

Phytoremediation is an in situ, solar-powered comprehensivestrategy for bioremediation of environmental problems by usingplants and their associated microorganisms to extract, sequester, ordetoxify pollutants. The plants mitigate the problems; environmen-tally invasive excavation of the contaminated material to dispose ofit elsewhere is avoided. Plants are able to contain, degrade, or elim-inate metals, pesticides, explosives, solvent, crude oil, and manyindustrial contaminants. Phytoremediation requires minimal dis-turbance and maintenance of a site and is a clean, cost-effective,environmentally friendly technology, especially for treatment oflarge contaminated areas with diffuse pollution. Many successfulexamples of phytoremediation are documented and employed inthe environmental cleaning industry (Macek et al., 2000; Sureshand Ravishankar, 2004).

The major disadvantage of phytoremediation is that phytoreme-diation requires a long-term economic commitment and patienceby project managers for results because the process is dependenton plant growth, tolerance to contaminants, and bioaccumula-tion capacity, all of which are slow processes. Phytoremediationinvolving a combination of several independent approaches mightshow an effect. These approaches include: (1) phytotransforma-tion, which reduces toxicity, inactivates, or degrades contaminantsresulting from plant metabolism; (2) rhizodegradation, whichenhances soil microbial activity to degrade contaminants by rhizo-sphere bacteria; (3) phytoextraction, which absorbs contaminantsfrom the polluted soils and stores the substances in the plantbiomass, with a potential to recover and re-use valuable metals,and (4) phytostabilization, which reduces mobility of toxic sub-stances in the soils, as in the case of mine tailings. All these benefitsnotwithstanding, on their own, plants have the disadvantage ofbeing inefficient. Even plants that are relatively tolerant of envi-ronmental contaminants often remain small in the presence ofcontaminants and remove only small quantities per plant. To obtainmore efficient degradation of organic compounds, plants depend ontheir associated microorganisms (Pilon-Smits and Freeman, 2006).To improve this process, inoculation with PGPB that enhance plantgrowth, especially under stressed conditions, offers advantages.Inoculation increases plant biomass, making phytoremediation afaster and efficient process and more attractive to the public (Glick,2003).

2.5. Phytodegradation, phytotransformation, bioaugmentation,rhizodegradation, and phytoextraction

Many organic pollutants are converted to harmless materialby the metabolism of plants and the rhizosphere microorganismsliving in association with the plant roots. Phytodegradation com-bined with bioaugmentation, microorganisms assisting the plants,(Lebeau et al., 2008) is defined as rhizodegradation. Root exu-dates provide a nutrient-rich environment where microbial activityis stimulated, which leads to more efficient degradation of pol-lutants. The root system also supports three-dimensional spread

of bacteria deeper into soils, penetrating otherwise impermeablesoil layers (Kuiper et al., 2001, 2004). Because some complex andrecalcitrant compounds cannot be broken down to basic molecules(water, CO2, volatile compounds) by plants or microbial enzymes,phytotransformation represents a change in chemical structureto a less harmful compound without complete breakdown of thecompound. In the final stage of phytotransformation, immobiliza-tion of the xenobiotic substance occurs within the plant, hence,phytoextraction. Phytoextraction also occurs by direct uptake ofthe contaminant if the metabolism of the plant is resistant toits toxicity. Xenobiotic substances are polymerized within theplant and develop a complex structure that is sequestered inthe plant and does not interfere with normal functioning of theplant (McCutcheon and Schnoor, 2003; Mukhopadhyay and Maiti,2010). In many cases, the effective solution combines severalof these processes. Because these techniques can last years ordecades, progress on many sites often includes combinations ofseveral techniques; therefore, it is difficult to estimate efficacyof bioremediation by each approach on large contaminated sites.Most published information deals with controlled and greenhouseexperiments.

2.6. PGPB for enhancing phytodegradation by increasingrhizoremediation

The rhizosphere contains microbial populations that are sev-eral orders of magnitude greater than the surrounding bulk soil;it is composed of numerous species capable of degrading xeno-biotic substances (Donnelly et al., 1994; Macková et al., 2007;Mendez and Maier, 2008). Along with higher capacity to degradesubstances, the rhizosphere of plants growing in contaminatedsoils may serve as a reservoir of PGPB. Because this is a rela-tively recent concept, there is little information in the scientificliterature. Related information, not scientifically peer-reviewed, isavailable on commercial websites. Kuiper et al. (2001) describesefficient root-colonizing, pollutant-degrading bacteria inoculatedon a suitable plant for phytoremediation, these bacteria settle onthe roots with the indigenous bacterial population and enhancedbioremediation. A combination of a plant and microbe was selectedthat led to efficient degradation of naphthalene and protectedgrass seed against high concentrations of naphthalene. In anothersoil, purposely contaminated with creosote, inoculation of tall fes-cue (Festuca arundinacea) with bacteria that degrades polycyclicaromatic hydrocarbons (PAH) and PGPB (Pseudomonas putida, A.brasilense, and Enterobacter cloacae), the rate of removal of PAHwas substantially increased. Large-sized PAH were removed in thepresence of these PGPB because these specific bacterial speciesmitigated stress in plants in general by ACC-deaminase activity,a common mechanism in PGPB (Huang et al., 2004). In anotherstudy, the PGPB, Pseudomonas spp., increased growth of the oilplant canola and common reed Phragmites australis in the pres-ence of copper or PAH (Reed and Glick, 2005; Reed et al., 2005). Instill another study, PGPB helped to degrade 2-chlorobenzoic acidand oil-contaminated soils for growing the broad bean Vicia fabaand several forage grasses, but no clear relationship between addeddisappearance of the pollutants and increased plant biomass wasfound (Radwan et al., 2005; Siciliano and Germida, 1997). Biore-mediation potential of the legume, goats rue Galega orientalis andits symbiont Rhizobium galegae was assessed in soils contaminatedwith benzene, toluene, and/or xylene (BTX). Good growth, nodula-tion, nitrogen fixation, and a strong rhizosphere occurred in soilscontaminated with oil or spiked with m-toluate, a model compoundrepresenting BTX (Suominen et al., 2000).

Similar to rhizosphere PGPB, many endophytic PGPB assisthost plants to overcome contaminant-induced stress, which pro-vided improved plant growth. In comparison with rhizosphere and



Fig. 5. Restrictions to large-scale applications of phytoremediation of organic pollutants and possible solutions.

phyllosphere PGPB, endophytic PGPB are likely to interact moreintimately with their host. During phytoremediation of organiccontaminants in soils, plants further benefit from their endophytes,which possess degradation pathways and metabolic capabilitiesnot inherent in the plant. This strategy leads to more efficient degra-dation and reduction of phytotoxicity and evapotranspiration ofvolatile contaminants (Weyens et al., 2009). For example, tall fes-cue F. arundinacea grass can selectively enhance the prevalenceof endophytes containing pollutant catabolic genes in environ-ments contaminated with different pollutants (hydrocarbons andnitro-aromatics). Enrichment of endophytic catabolic genotypes isplant- and contaminant-dependent (Siciliano et al., 2001). Baracet al. (2009) found that, when remediation reduced BTX belowdetectable levels, the capacity of the endophytic community inpoplars to degrade BTX disappeared. When the pea plant Pisum

sativum was inoculated with an endophyte originated from poplarand capable of degrading the herbicide 2,4-D, it increased removalof 2,4-D from the soil (Germaine et al., 2006).

There are several restrictions for large-scale application of phy-toremediation of organic pollutants: (1) limits to the concentrationof contaminants that can be tolerated by plant species; (2) fre-quently, contaminants are not bio-available; and (3) dispersal ofthe contaminant to the atmosphere (volatization) is not alwaysacceptable. The use of task-specific, genetically engineered plantsand modifying the rhizosphere for accelerated rhizodegradationof persistent organic contaminants may solve these difficulties(Doty, 2008; Dzantor, 2007). If no naturally occurring endophytesare available that have the desired metabolic properties, generalendophytic bacteria can be isolated from the plants. The neededdegradation pathways can be added to these endophytes by genetic



manipulation and these modified endophytes can be inoculatedby vacuum infiltration (Puente and Bashan, 1993) into the seedsof the host plants to serve as PGPB. Engineered endophytes willimprove phytoremediation by complementing the metabolic prop-erties of their host plant. Evidence for this approach was providedby inoculating yellow lupine Lupinus luteus (Barac et al., 2004) andpoplar Populus sp. (Taghavi et al., 2005) with endophytic bacte-ria able to degrade toluene. This reduced toluene phytotoxicityand significantly lowered evaporation of toluene. In another study,a plasmid was transferred from Burkholderia cepacia to an endo-phytic PGPB strain of this species and this protected the new hostagainst toluene toxicity and reduced evaporation of toluene (Glick,2004). Newman and Reynolds (2005) engineered endophytes thatincreased plant tolerance to toluene and decreased transpiration oftoluene to the atmosphere.

In summary, rhizosphere and endophytic PGPB have potentialto enhance biodegradation of organic pollutants. The advantages ofendophytic PGPB over rhizosphere PGPB give additional perspec-tive in the use of the former as the method of choice for furtherdevelopment.

2.7. Phytoextraction

Phytoextraction (also known as phytoaccumulation, phytoab-sorption, and phytosequestration) is a green in situ technologythat uses plants to remove contaminants from the environment byconcentrating them within the biomass of the plant. The processhas been studied mostly for extraction of heavy metals from soilsand water containing moderate concentrations of contaminants.The purpose for this technology is to reduce concentrations of met-als in contaminated soils to a level that permits the soil to be usedwithout danger in agriculture, horticulture, forestry, grazing, orurban uses. Within the plant biomass, the contaminant is more con-centrated than in the environment, which facilitates safe disposal.Phytoextraction is best performed by growing plants that are highlymetal-accumulating, the so-called hyper-accumulators. These areplants that can tolerate and absorb higher amounts of toxic met-als than most plants. A conditioning fluid containing a chelator,which enhances mobilization of metals may be applied to a con-taminated site to mobilize the metals and help the plants absorbthe metals more easily. So far, large transgenic plants have shownno advantage in phytoextraction, compared to the high potentialof genetically unmodified plant species (Cunningham et al., 1995;Ernst, 2005; Pilon-Smits, 2005). The limitations of phytoextraction,such as bioavailability, uptake, and toxicity are well recognized andrequire significant optimization steps to make it a widely usefultechnology (Lebeau et al., 2008).

Phytoextraction is usually a long-term process that cannotentirely eliminate the contaminant (Fig. 5). Extraction has beendemonstrated only for some metals. Although numerous plants canserve as metal absorbers to some extent, many of the 400 knownhyper-accumulating plant species belong to the Brassicaceae fam-ily with some plants in an additional 10 families (Gratão et al.,2005; Nanda Kumar et al., 1995; Prasad and Freitas, 2003). Geneticmanipulation of plants and its associated microbial communities(rhizosphere engineering) has been proposed to optimize phytoex-traction. These include: isolation of competent plant-associatedrhizosphere bacteria and loading them with metabolic pathwaysthat allow the synthesis of natural chelators to improve metalbioavailability or sequestration systems to reduce phytotoxicity.This is followed by inoculating the genetically changed bacte-ria to plants growing on contaminated soils (Lodewyckx et al.,2001; Valls and de Lorenzo, 2002). Endophytes possessing a metal-resistance or sequestration system can lower metal phytotoxicityof the plants and transfer metals to aerial parts (Weyens et al.,2009).

Some examples demonstrate this principle: uptake of cadmiumand zinc by the hyper-accumulating perennial herb Sedum alfrediican be increased after plants are inoculated with endophytic bacte-ria equipped with the appropriate metal-resistance/sequestrationsystem (Li et al., 2007). When yellow lupin L. luteus was grownon a nickel-enriched substrate and inoculated with the engineerednickel-resistant endophytic bacterium B. cepacia, there was a 30%increase of nickel in the roots, whereas nickel in the aerial partsremained comparable with control plants (Lodewyckx et al., 2001).Since plants absorb contaminants from soil or water through roots,biological factors that modify root metabolism and enlarge the rootsystem, such as inoculation with PGPB, can enhance phytoextrac-tion (Ma et al., 2011; Stout and Nüsslein, 2010). AM fungi have beensuggested for improving phytoextraction (Cornejo et al., 2008; Faet al., 2007), but this topic is outside the scope of this review.

Depending on the economic value of the metal, accumulatedtoxic metals in hyper-accumulators can be harvested for metalrecovery and the leftover biomass composted. On the less favorableside of phytoextraction, apart from inherent capacity to accumulatecontaminants, many hyper-accumulators produce a small biomassand have limited ability to extract more than one or two met-als. They are also sensitive to other metals that are present inabundance. In heavily contaminated soils, growth of these plantscan be retarded or have minimal uptake so that phytoextractionprojects become impractical. Inoculation with phytostimulatingPGPB might be a solution in these cases.

PGPB and AM fungi improve rates of phytoextraction in twomain ways: (1) enhance general growth of plant. With a largerbiomass, more contaminants can be absorbed; and (2) increasemetal mobilization by microbial metabolites (Lebeau et al., 2008).The ideal PGPB might do both (Rajkumar and Freitas, 2008a,b;Saravanan et al., 2007; Sheng and Xia, 2006), but usually onemechanism in each microorganism was studied. There are manyexamples demonstrating these abilities. Inoculation with rhizobiaenhanced dry plant biomass of soybean in arsenic-contaminatedsoils (Reichman, 2007). Root elongation of ferns and arsenic accu-mulation increased after inoculation with rhizospheric bacteria(Jankong et al., 2007). Aerobic bacteria Variovorax spp. enhancedroot elongation of Indian mustard (Brassica juncea) in the presenceof cadmium (Belimov et al., 2005). Following inoculation with bac-terial strains, large increases in several metals were sequesteredwithout enhancing biomass (Brunetti et al., 2011; Hoflich andMetz, 1997; Rajkumar and Freitas, 2008a,b; Reed and Glick, 2005;Whiting et al., 2001). Inoculation might improve overall plant nutri-tion, as is common of PGPB. Several rhizosphere strains enhancedvolatilization and accumulation of selenium and mercury in planttissues in an artificially constructed wetland (de Souza et al.,1999a,b). Under hydroponic conditions, simultaneous addition ofEDTA and indole-3-acetic acid (IAA) synthesized by rhizobacte-ria increased extraction of lead by a factor of 28, in contrastto only a factor of 6 with EDTA (Lopez et al., 2005). Severalisolates of rhizosphere bacteria with common plant growth-promoting traits enhanced extraction of cadmium and zinc bywillow seedlings using a variety of mechanisms, but not by produc-ing IAA and 1-amino-cyclopropane-1-carboxylic acid deaminase(ACC deaminase), which are common mechanisms in agriculturalPGPB (Kuffner et al., 2008). A surprising finding was that in vitroexperiments of mobilization of metals predicted the effects ofbacteria on willows more reliably than standard tests for plantgrowth-promoting activities (Kuffner et al., 2010). A similar caseinvolved three rhizosphere bacteria isolated from the root of thehyper-accumulator yellowtuft Alyssum murale, an annual that sig-nificantly increased uptake of nickel into the aerial parts, whileuntreated plants had no positive effect on extracting nickel fromsoil (Abou-Shanab et al., 2003). When the hyper-accumulator S.alfredii was inoculated with B. cepacia, growth, uptake of metal,



greater translocation of metals from root to shoot, and stimula-tion of organic acid secretions occurred. There appears to be afunctional resistance to metals that chelate metal ions extracel-lularly, which reduces uptake and subsequent deleterious effecton physiological processes in the root (Li et al., 2007). Increases insolubilization of metals and subsequent plant uptake of these con-taminants may be the result of organic acid production by somePGPB (Saravanan et al., 2007). Many PGPB that are phosphate sol-ubilizers produce organic acids (Lopez et al., 2011; Puente et al.,2004a,b; Rodriguez et al., 2004, 2006; Vazquez et al., 2000). Sev-eral PGPB (Pseudomonas aeruginosa, Pseudomonas fluorescens, orRalstonia metallidurans) that are able to produce siderophores wereintroduced to a maize field containing chromium and lead. R. metal-lidurans enhanced accumulation of chromium in the maize shootsby a factor of almost five; similarly, P. aeruginosa increased uptakeof chromium into maize shoots at the same rates, but not in theirroots. Consequently, total uptake of metal by the whole plant usu-ally decreases after inoculation with these bacteria (Braud et al.,2009).

PGPB can provide protection to plants against metal toxicity.For example, Kluyvera ascorbata, which contains the enzyme ACCdeaminase, protects Indian mustard B. juncea and rapeseed Brassicacampestris against nickel, lead, and zinc toxicity (Burd et al., 1998),probably by reducing the stress caused by high ethylene content.Root elongation of rapeseed Brassica napus is also stimulated by theIAA that is synthesized by PGPB in soil contaminated with cadmium(Sheng and Xia, 2006), as was an unidentified rhizobacterium onIndian mustard roots (Belimov et al., 2005).

The best-studied PGPB are Gram-negative bacteria, but someGram-positive PGPB are also known for excellent biocontrol, plantgrowth promotion, and bioremediation activity (Francis et al.,2010). For example, at sites contaminated with nickel, inoculationof Indian mustard with B. subtilis yielded high concentrations ofnickel in the plant tissues and increased plant biomass. This resultsfrom a combined effect of bacterial hormone production, solubi-lization of inorganic phosphate, and adsorption of nickel (Khanet al., 2009). Inoculation of Indian mustard with a nickel-tolerantB. subtilis significantly enhanced plant growth and produced a pro-tective effect against phytotoxicity from nickel, probably throughinvolvement of IAA in uptake of the metal (Zaidi et al., 2006). B.pumilus and Rhodococcus spp. increased plant biomass, but not theamount of metals accumulated by plants (Belimov et al., 2001,2005; Safronova et al., 2006).

Some PGPB can degrade pollutants or prevent their accumu-lation in plant tissues. In soil contaminated with heavy metals,Arthrobacter mysorens, which is resistant to cadmium and lead, canimprove plant growth in the rhizosphere of barley and preventaccumulation of heavy metal in the plant tissues. Several Bacil-lus strains isolated from chromium-contaminated soil reduced thehighly toxic, mutagenic, and carcinogenic Cr6+ to the less toxic Cr3+

(Khan et al., 2009). Psychotrophic Rhodococcus erythropolis that wasisolated from a metal-contaminated site in the Himalayas had plantgrowth-promoting traits and an ability to reduce chromate at lowtemperatures of ∼10 ◦C (Trivedi et al., 2007).

Excretion of root exudates can stimulate growth of spe-cific, pollutant-degrading bacteria in the rhizosphere by secretingphospholipid surfactants that make organic pollutants more bio-available or by releasing secondary metabolites that induceexpression of genes with a capacity to degrade organic pollutants(Pilon-Smits, 2005). For example: Rhodococcus spp. were themost common group in the rhizosphere of trees that naturallycolonized and improved a PCB-contaminated site in the CzechRepublic (van der Geize and Dijkhuizen, 2004). Barley growingin PAH-contaminated soils supported growth of a Mycobacteriumspecies capable of mineralizing the PAH (Child et al., 2007). Soilscontaminated with petroleum derivatives typically contain high

concentrations of m-toluate. Although Pseudomonas spp. are thebest m-toluate degraders in the rhizosphere of oriental goat’s rueG. orientalis grown on these soils, most isolates were Gram-positivestrains of the genera Rhodococcus, Arthrobacter, Bacillus, and Nocar-dia (Jussila et al., 2006).

In summary, phytoextraction of heavy metals and a few othercontaminants show promise, but not much capacity on a largerscale than the laboratory and greenhouse. To optimize phytoex-traction, a contaminated site should be considered as a large-scalebioreactor supported by an approach where the microbial pop-ulation of the rhizosphere is genetically engineered. Large-scaledevelopment of phytoextraction will depend on: (1) reliabilityand repeatability of the process, which yet needs to be demon-strated; (2) ease of application needs to be similar to that forrhizobia and PGPB applied in agriculture; (3) capacity to clean uppoly-contaminated soils; and (4) economic value demonstrated bycomparing microorganism-assisted plants or plants not assistedby microorganisms, as well as whether PGPB promote or do notpromote plant growth under adverse conditions.

2.8. Phytostabilization

Phytostabilization (also known as in-place inactivation or phy-toimmobilization) is a long-term, unobtrusively green, in situapproach to contain contaminants. When a soil is highlycontaminated with more than one metal (polymetallic soils), phy-toextraction (described above) will last decades or more; thus,this period is too long for an economically feasible technology(Ernst, 2005). Phytostabilization can occur through metallic sorp-tion, precipitation, complexing, or reduction of toxicity. The basisfor phytostabilization is that metals do not degrade, so capturingthem in situ is sometimes the best alternative at sites with lowcontamination levels or vast contaminated areas where large-scaleremoval or other in situ remediation is uneconomical. There is con-sensus that it is better to restrict a contaminant in one area thanto allow it to disperse to uncontaminated areas. A vegetative capthat is sufficiently dense to prevent wind erosion and roots thatreduce water erosion can prevent dispersal to nearby urban andagricultural areas and into aquifers. Plants may restrict pollutantsby creating a zone around the roots where the pollutant is precipi-tated and stabilized. Phytostabilization does not absorb pollutantsinto plant tissue, but sequesters pollutants in soil near the roots,becoming less bio-available and reducing exposure to humans, live-stock, and wildlife. The most common application is containment ofmine tailings (McCutcheon and Schnoor, 2003; Mench et al., 2006;Mendez and Maier, 2008; Mukhopadhyay and Maiti, 2010; Petrisoret al., 2004; Xue et al., 2009; Zhuang et al., 2007).

2.8.1. PGPB in programs for phytostabilization of mine tailingsMainly in deserts, wind-blown toxic dust and pollution of

ground water from large mounds of tailings from abandoned andproducing mines are potentially a long-term health hazard tonearby urban populations. Tailings, lacking plant cover and soilstructure, are easily transported by wind and rain; thus, tailingsserve as a continuous source of metallic pollution (Pilon-Smits,2005). Phytostabilization is an economical strategy for using nativeplants as ground cover to prevent erosion and reduce health haz-ards (McCutcheon and Schnoor, 2003). A major challenge is thatmost tailing deposits cannot serve as a substrate for most plantspecies because of metal toxicity, low pH, lack of essential minerals,lack of clay and organic matter to retain water, lack of soil structure,or lack of a seed source from nearby native plants or some com-bination of these factors (Mendez and Maier, 2008). Tailings canremain devoid of plants for many decades or, in some cases, haveonly slight plant cover (Gonzalez-Chavez et al., 2009). One approachto modify the inhospitable substrate into a soil-like status can be



accomplished by adding large quantities of compost, biosolids, andwater (Ye et al., 2001; Chiu et al., 2006). Though theoretically feasi-ble, amendments become costly if applied to extensive areas withtailings. Frequently, these sites are remote and water and irrigationfacilities are absent, especially at long-abandoned mine sites.

A more practical alternative is to use pioneering plants, mainlyleguminous shrubs and trees that fix nitrogen. This initial stageimproves soil characteristics by adding organic content and mayreduce soil toxicity. Later, more sensitive plants may grow; this cre-ates a more stable and diversified ecosystem. One suitable pioneerlegume is the genus Sesbania, which tolerates detrimental effectsof heavy metals and supplies much-needed nutrients to the soilas it decomposes, especially nitrogen (Chan et al., 2003). Inocula-tion with PGPB and also AM fungi has been proposed to supportcultivation of plants on tailings using smaller amounts of compost(Mendez and Maier, 2008; Petrisor et al., 2004; Solís-Domínguezet al., 2011; Zhuang et al., 2007) (Fig. 6).

There are two approaches in the search for PGPB compatiblewith mine tailings. One is to isolate native PGPB from tailings orfrom plants already growing on tailings, culture the bacteria, anduse them as inoculants. This is a labor intensive procedure thathas been successfully tested (Grandlic et al., 2008, 2009). Thisapproach assumes that the PGPB isolated from tailings providebetter support for plant survival and growth through several mech-anisms, including increasing availability of nutrients, increasingresistance to metal toxicity, or decreasing bioavailability of toxicmetals in the rhizosphere (Burd et al., 1998, 2000; Pishchik et al.,2002; Glick, 2003; Belimov et al., 2004; Reed and Glick, 2005; Reedet al., 2005; Vivas et al., 2006; Wu et al., 2006a; Li et al., 2007;Rajkumar and Freitas, 2008a,b). Another approach is to test well-studied PGPB used in other applications, mainly agriculture, thatcould help plants grow on mine tailings. For example, strains ofBacillus enhance growth of agricultural crops, wild plants, trees,microalgae, and test plants by means of different mechanisms ofplant growth (Bashan et al., 2000b; Enebak et al., 1998; Hernandezet al., 2009; Kloepper et al., 2004a,b; Ryu et al., 2005; Vessey,2003). Also, strains of Bacillus are found in mine tailings (Natarajan,1998; Vijayalakshmi and Raichur, 2003; Wu et al., 2006b; Tsuruta,2007). The genus Azospirillum is commonly used for its growth-promoting activities and is probably the best studied of the PGPB,except for rhizobia (Bashan and de-Bashan, 2010). Root stimulationand reduced salt stress are common concerns in phytostabiliza-tion of mine tailings in semi-arid and arid ecosystems. Stimulationof adventitious root growth by A. brasilense enhances nutrientuptake, but also alleviates salt stress in agricultural plants (Bashanet al., 1999; Bacilio et al., 2004; Creus et al., 1997; Dimkpa et al.,2009). This stimulatory action provides increased surface area forabsorbing nutrients in the highly impacted, low-nutrient depositsof tailings. Increased root mass also adds physical stability againstwind and water erosion. In addition to promoting plant growthand enhancing resistance to abiotic stress, properties of Azospiril-lum that are relevant for their use include the ability to grow underextremes of pH (de-Bashan et al., 2005) and heavy metals (Belimovand Dietz, 2000).

Another alternative available with legumes is inoculation withrhizobia. Several species of Sesbania were tested for remediationof tailings containing lead, zinc, and copper. Inoculated plantsgenerally produced a higher biomass than plants that were notinoculation (Chan et al., 2003). Yellow lupine L. luteus was testedfor in situ reclamation of multi-metal-contaminated soil after amine water spill. It accumulated heavy metals mainly in roots;however, lead, copper, and cadmium were not well translocatedto shoots. This demonstrated that yellow lupine is potentially use-ful in metal phytostabilization. Inoculating lupines with a mix ofmetal-tolerant PGPB (Bradyrhizobium spp., Pseudomonas spp., andOchrobactrum cytisi) produced further increase in biomass. At the

same time, metal accumulation in shoots and roots declined, whichmay have resulted from a protective effect that the PGPB exertedon the plant rhizosphere (Dary et al., 2010).

While there is a similarity in the concepts of phytostabiliza-tion and revegetation of severely eroded areas mentioned earlier,the main differences involve presence of toxic metals and some-times extreme pH of the tailings. Several studies demonstratedthe benefits of using native PGPB to enhance plant growth in phy-tostabilization projects (Grandlic et al., 2008, 2009; Petrisor et al.,2004; Vivas et al., 2006). These PGPB can significantly increase rootand shoot length, biomass, and improve overall plant nutrition,despite the presence of heavy metals. These fairly new studies pro-pose mechanisms used by bacteria to improve vegetative growth,similar to mechanisms of PGPB employed in agriculture: (1) PGPBwith ACC-deaminase activity stimulate root elongation and gen-eral plant growth in soils containing cadmium, but do not enhanceextraction of metals (Belimov et al., 2001); (2) PGPB alleviate heavymetal toxicity by reducing sensitivity of plants to higher concentra-tions of cadmium, copper, zinc, and nickel, yet reduce absorptionof the metals by the plants (Belimov et al., 2004; Burd et al., 1998;Reed et al., 2005; Vivas et al., 2006).

Several studies demonstrate the feasibility of using PGPB forphytostabilization; some were done in combination with compost.Some studies show that the optimal quantity of compost for estab-lishment of several species of grasses and plants on tailings can bereduced by using PGPB that were isolated from tailings or areas neartailings (Grandlic et al., 2008; Petrisor et al., 2004; Zhuang et al.,2007). In one study, chemical fertilizer was replaced with repeatedinoculations of Azotobacter chroococcum and Bacillus megaterium;this significantly enhanced the growth of native species and micro-bial activity in two acidic tailing sites (Petrisor et al., 2004). Severalstudies used desert shrubs and trees to demonstrate the capac-ity of native and commercial PGPB to improve growth of severaltypes of mine tailings. PGPB isolated from these tailing survivedstrong acidic pH and high concentrations of heavy metals (Mendezet al., 2008). When moderate amounts of compost was added withthe PGPB (Iverson and Maier, 2009), biomass of desert quailbushAtriplex lentiformis and buffelgrass Buchloe dactyloides significantlyincreased. Inoculating seeds of these plants with PGPB prior toplanting resulted in significantly increased dry biomass of nativedesert plants raised on sulfurous tailings, some even without com-post. The effect was partly dependent on the amount of the compostamendment (Grandlic et al., 2008, 2009; Iverson and Maier, 2009).Similarly, when quailbush was inoculated with B. pumilus iso-lated from roots of cacti growing on soilless rocks in an extremeenvironment, the bacterium significantly improved the growth ofquailbush with a smaller amount of compost (10% w/w comparedto 15% normally used on these tailings). This treatment markedlyaffected the bacterial community of acidic tailings with high metalcontent and with neutral tailings with low metal content (de-Bashan et al., 2010a). Using several strains of A. brasilense usedin agricultural applications caused similar effects on plant growthand the microbial community in acidic, metalliferous tailings (de-Bashan et al., 2010a,b). Inoculation of buffelgrass with a mix oftwo PGPB (Arthrobacter spp.) changed the structure of rhizospherebacterial communities; after 75 days, the inoculants had increasedgrowth of buffelgrass (Grandlic et al., 2009).

There are at least two plausible explanations for the effectof inoculation on bacterial communities in tailings that are notapparent when these bacteria are added to agricultural soils.Tailings usually have extremely low content of heterotrophicbacteria (<103 CFU g−1) (Mendez et al., 2007). With a relativelysmall community of bacteria, inoculation of either B. pumilusor A. brasilense (∼106 CFU g−1) creates a large shift in the com-position of native bacteria. Additionally, PGPB have an indirect,but long-term effect on the native bacterial population because



Fig. 6. Proposed process of phytostabilization of mine tailings.

the inoculum influences root growth or plant exudates after theinitial population of PGPB declines (de-Bashan et al., 2010a,b).Long-term influence (5 years) on growth of cacti and desertleguminous trees in impoverished soils occurred, even when theinitial inoculum had disappeared years earlier (Bashan et al., 1999,unpublished).

Because some leguminous trees tolerate soils that are contam-inated with heavy metals (Senthilkumar et al., 2005), they arecandidates for revegetation of tailings. Inoculation with Bradyrhizo-bium sp. of the leguminous lebbeck tree Albizia lebbeck significantlyincreased nodulation and various growth parameters grown ongypsum and limestone tailings (Rao and Tak, 2001). Although inoc-ulation sometimes enhances metal uptake in mesquite, this did nothappen when several AM fungi were inoculated onto mesquitegrowing on acidic tailings containing high levels of heavy met-als (Solís-Domínguez et al., 2011). Inoculation with a combinationof the PGPB A. brasilense, AM fungi, and compost significantlyenhances growth of seedlings of the mesquite amargo on phos-phate mine tailings (Moreno et al., unpublished data) similar to theeffect of AM fungi on this tree.

The end goal of phytostabilization, as part of general phytore-mediation, is not only to establish a vegetative cap to stabilize metalcontaminants in the root zone, but to modify the soil to enhanceplant succession, that is, support a diversity of native plants closeto the natural vegetation of local soils (Fig. 6). Ideally, a transitionwould include a more diverse indigenous microbial community,one capable of supporting plant growth and nutrition. Inoculationwith PGPB used in agriculture enhances plant growth when supple-mented with compost and enhances continued ecological impactson the rhizosphere microbial community. These are distinctly dif-ferent from the microbial community residing on uninoculatedplants. Also, plants that have not been inoculated have less robustaerial and root growth.

A potential negative impact of using PGPB for phytostabiliz-ing mine tailings occurs when toxic metals accumulate in aerial

parts of plants, rendering the plants toxic to grazing animals. Forexample, roots of Indian mustard B. juncea inoculated with PGPBhad minor absorption of copper, lead, and zinc, but significantlyincreased cadmium uptake in shoots (Wu et al., 2006a,b). Copper,cadmium, manganese, and zinc increased in shoots of native plantsafter inoculations (Petrisor et al., 2004). In still another study, afterinoculation, concentrations of heavy metals accumulated in shootsof canola, which can happen when canola is grown on soils withlow concentrations of metal. The low concentration was toleratedby canola (Reed and Glick, 2005).

In summary, for hostile environments, such as toxic mine tail-ings, an inoculant PGPB can not only persist and stimulate plantgrowth but directly or indirectly influence development of rhi-zobacterial communities. A PGPB can be native to the tailingsor a common agricultural inoculant. PGPB can be a componentof phytostabilization programs, together with compost and suit-able plants that do not accumulate metals in their shoots toavoid poisoning grazing animals. This is the most viable optionfor achieving coverage of toxic tailings. Part of this processis to understand the relationship between PGPB and organicamendments or find plant–PGPB combinations that do not needcompost.

2.9. PGPB to improve tertiary wastewater treatment

Tertiary treatment of wastewater is done mainly by chemicalprecipitation and, to a lesser extent, by biological means, suchas bacteria and microalgae, but only to a limited extent becausemost wastewater only receives secondary treatment (digestion oforganic matter) before it is discharged or sold for irrigation (de-Bashan and Bashan, 2010). Developing efficient and cost-effectivetreatments have major significance because common contami-nants are increasing. Most wastewater treatment facilities willface these issues in the near future. Numerous species of microal-gae are commonly used to remove nitrogen and phosphorus



in municipal wastewater (Tam and Wong, 2000; Valderramaet al., 2002). PGPB are not employed in current technologies.The idea of using PGPB for wastewater treatment came fromtesting if microalgae respond to PGPB application in ways simi-lar to higher plants. Because microalgae are basically single-cellplants, as plants they may respond to PGPB application as doother plants. The concept of an association of the microalgaeChlorella vulgaris and the PGPB A. brasilense in alginate beads wasdeveloped as part of the phycoremediation approach (de-Bashanand Bashan, 2008; Gonzalez and Bashan, 2000). This combina-tion is highly efficient at removing nitrogen and phosphorusfrom several types of wastewater to prevent algal blooms, leaveswater cleaner, and provides a waste of usable biomass (de-Bashanet al., 2002a, 2004). When immobilization of two microorgan-isms is undertaken (also known as co-immobilization), microalgaeremove contaminants and the PGPB enhances its capacity toabsorb these nutrients by changing metabolism and prolifera-tion.

The effectiveness of using the microalgae C. vulgaris and Chlorellasorokiniana immobilized with the well-known PGPB A. brasilensein alginate beads under diverse environmental conditions wasintensively studied in recent years (de-Bashan et al., 2002a,b,2004, 2005, 2008a, 2011; Gonzalez and Bashan, 2000; Lebskyet al., 2001) (Fig. 7). A few other studies have also demonstratedthat other bacterial genera, including Rhodanobacter, Pseudomonas,Bacillus, and Paenibacillus may advance wastewater treatment(Hernandez et al., 2009; Mouget et al., 1995; Ogbonna et al.,2000).

Early studies showed that A. brasilense increased growth rate,population size, and lifespan of C. vulgaris by delaying senescence(Gonzalez and Bashan, 2000; Lebsky et al., 2001). By immobiliz-ing this microalga with A. brasilense, almost all ammonium andabout one-third of the phosphorus was removed after 2 days

of incubation in a batch culture, compared to using only C. vul-garis cells (de-Bashan et al., 2002a). A. brasilense has beneficialeffects on parameters of microalgae growth, including increasedproduction of pigments, lipid content, changing pattern of appear-ance of fatty acids in the cells, increased number of microalgalcells, and sometimes, larger cell size (de-Bashan et al., 2002b).A. brasilense Cd consistently enhanced growth of C. sorokinianaor C. vulgaris, removed ammonium from wastewater, and slightlyreduced nitrates (de-Bashan et al., 2004).

To improve synergism between the two microorganisms, sev-eral environmental factors that affect growth of microalgae andits cellular mechanisms were explored. These factors included pH,concentration of carbon and nitrogen (affects nitrogen uptake in C.vulgaris cells), light intensity at high temperature, and presence oftryptophan. Hormonal effects were also evaluated (de-Bashan andBashan, 2008; de-Bashan et al., 2005, 2008a,c). A. brasilense allevi-ated tryptophan toxicity and extreme pH (de-Bashan and Bashan,2008; de-Bashan et al., 2005). These physiological studies indicatethat a plausible mechanisms controlling growth is production ofthe phytohormone IAA and enhancement of two key enzymes (glu-tamate dehydrogenase and glutamine synthetase) that affect thenitrogen cycle and are also responsible for absorbing ammoniuminto the microalga (de-Bashan et al., 2008b).

Starvation periods have a profound effect on assimilatingphosphorus from wastewater by C. vulgaris and C. sorokinianaimmobilized with A. brasilense. Joint immobilization enhancedgrowth and absorption of phosphorus in both microalgae in syn-thetic wastewater and in C. sorokiniana in municipal wastewaterfollowing a 3-day starvation in a saline solution. Phosphorusremoval did not increase after a starvation period and return ofthe microalgae to the same wastewater; however, if cells werereturned to a new batch of wastewater, removal of phosphoruscontinued. The most effective removal of phosphorus (72%), about

Fig. 7. PGPB (Azospirillum spp.) that are jointly immobilized with microalgae (Chlorella spp.) in alginate beads to improve tertiary wastewater treatment under authotrophicand heterotrophic conditions. Abbreviations: Azo = Azospirillum spp., Ch = Chlorella spp., GS = glutamine synthetase, GDH = glutamate dehydrogenase, IAA = indole-3-aceticacid, P-ase = phosphatase.



double the rate of common removal of phosphorus by suspendedbacteria or microalgae, was achieved when starved, immobilizedcells of microalgae and bacteria were used for treatment for onecycle and replaced with a fresh, starved culture (Hernandez et al.,2006). When cultivation was changed to heterotrophic conditions(without light and with an additional simple carbon source, glu-cose or acetate), the system of microalgae and bacteria performedbetter (Perez-Garcia et al., 2010). To improve fertility of desertsoils containing very little organic matter; the dried debris of algi-nate beads containing C. sorokiniana and A. brasilense from tertiarytreatment of wastewater was used as an amendment. Three appli-cations of debris increased organic matter, organic carbon, andmicrobial carbon in the soil. Sorghum grew better in the amendedsoil than sorghum grown in unfertile, untreated soil (Trejo et al., inpress).

The advantage of this technology is that immobilized cells ofmicroalgae with bacteria are always more effective at remov-ing nitrogen and phosphorus than microalgae without bacteria.As the two microorganisms are immobilized in alginate beadsthat are easily and rapidly removed from wastewater by sedi-mentation, this technology could be a cost-effective alternativeto chemical precipitation used to treat wastewater. It solves twoproblems in standard microalgal technology, increasing the popu-lation of microalgae to a level sufficient to clean the wastewater,and using the waste biomass when the cleaning process is com-pleted.

3. Conclusions and future prospects

Bioremediation is recognized as a suitable tool, yet not a widelyused approach, to restore contaminated sites, reforest eroded areas,and restore degraded ecosystems. The plant that is the major com-ponent of the phytoremediation processes. PGPB may serve asvaluable components in bioremediation of contaminated soil andwater and revegetation and reforestation of degraded lands. Ontheir own, a few bacterial strains can serve to remediate a soilwhen cultivated as large populations. However, their fullest poten-tial usefulness is their close association and positive influence onplant growth and function.

PGPB can be employed in distinct areas of bioremediation; itmay be useful to conclude by specifically addressing the area inquestion and avoid generalizations that may not be applicable.(1) PGPB and AM fungi can be successfully employed in revegeta-

tion and reforestation programs. However, applications shouldconsider the inherent limitations of PGPB that work best onseedlings and initial stages of plant growth, while rhizobia andAM fungi can establish a long-lasting association with treesand shrubs used in these programs. The positive plant–PGPBinteractions are probably effective at the plant–bacteria level.Inoculation by a consortium is not the norm. Each combinationof plant species, PGPB, and AM fungi should be tested sepa-rately.

(2) PGPB obtained from mangrove rhizospheres can be used toenhance reforestation with mangrove seedlings and restora-tion of mangrove ecosystems. This can be done by inoculatingseedlings with PGPB participating in one or more of the micro-bial cycles of the ecosystem.

(3) Rhizosphere and endophytic PGPB have demonstrated theircapacity to enhance biodegradation of organic contaminants,where endophytic PGPB have an advantage.

(4) Phytoextraction of heavy metals and a few other contaminantswith or without PGPB is so far limited.

(5) Phytostabilization of mine tailings with the addition of PGPBis currently very limited in practice. PGPB may be native of thetailings or be a common agricultural inoculant. A small additionof compost with PGPB inoculation is mandatory because PGPB

species tested so far are not effective on enhancing plant growthwithout adding organic matter.

(6) Immobilization of PGPB with microalgae in small polymerspheres (beads) was effective in bioremediation of wastewater.There is still no example of scaling up of this procedure.

A few general future prospects can be suggested for PGPB tech-nology. PGPB can be developed for sustainable production of biofuelcrops in conjunction with phytoremediation of contaminated soilsand water or to improve revegetation and sustainable feedstockproduction on marginal lands. With growing knowledge of com-plete genome sequences for many PGPB, exploitation of these datashould center on functional analysis of bioremediation questionsinvolving the genes, proteins, and metabolites in the PGPB. In sum-mary, PGPB has major potential in bioremediation problems, butthe past efforts are only the beginning.

Acknowledgments

This review was mainly supported by the Consejo Nacional deCiencia y Tecnología (CONACYT grant 130656) and the Secretaria deMedio Ambiente y Recursos Naturales, (SEMARNAT grant 23510).Time for writing was provided by The Bashan Foundation, USA. IraFogel of CIBNOR provided editorial services.

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