CorrespondenceseemabhargavsharmagmailcomDepartmentofEarthandEnvironmentalScienceKSKVKachchhUniversityMundraRoadBhuj370001GujaratIndiaFulllistofauthorinformationisavailableattheendofthearticle ID: 138662
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REVIEWOpenAccess Phosphatesolubilizingmicrobes:sustainable approachformanagingphosphorusdeficiencyin agriculturalsoils SeemaBSharma 1* ,RiyazZSayyed 2 ,MrugeshHTrivedi 1 andThivakaranAGobi 3 Abstract Phosphorusisthesecondimportantkeyelementafternitrogenasamineralnutrientintermsofquantitativeplant requirement.Althoughabundantinsoils,inbothorganicandinorganicforms,itsavailabilityisrestrictedasit occursmostlyininsolubleforms.ThePcontentinaveragesoilisabout0.05%(w/w)butonly0.1%ofthetotal Pisavailabletoplantbecauseofpoorsolubilityanditsfixationinsoil(IllmerandSchinner,SoilBiolBiochem layingdowntheprimordiaofplantreproductiveparts.Itplayssignificantroleinincreasingrootramificationand strengththerebyimpartingvitalityanddiseaseresistancecapacitytoplant.Italsohelpsinseedformationandin earlymaturationofcropslikecerealsandlegumes.Pooravailabilityordeficiencyofphosphorus(P)markedly reducesplantsizeandgrowth.Phosphorusaccountsabout0.2-0.8%oftheplantdryweight. Tosatisfycropnutritionalrequirements,PisusuallyaddedtosoilaschemicalPfertilizer,howeversynthesisof chemicalPfertilizerishighlyenergyintensiveprocesses,andhaslongtermimpactsontheenvironmentinterms ofeutrophication,soilfertililitydepletion,carbonfootprint.Moreover,plantscanuseonlyasmallamountofthis Psince75 90%ofaddedPisprecipitatedbymetal cationcomplexes,andrapidlybecomesfixedinsoils.Such environmentalconcernshaveledtothesearchforsustainablewayofPnutritionofcrops.Inthisregards phosphate-solubilizingmicroorganisms(PSM)havebeenseenasbesteco-friendlymeansforPnutritionofcrop. Although,severalbacterial( pseudomonadsandbacilli )andfungalstrains( Aspergilli and Penicillium )havebeen identifiedasPSMtheirperformanceunder insitu conditionsisnotreliableandthereforeneedstobeimprovedby usingeithergeneticallymodifiedstrainsorco-inoculationtechniques.ThisreviewfocusesonthediversityofPSM, presentandfuturescenariooftheiruseandpotentialforapplicationofthisknowledgeinmanagingasustainable environmentalsystem. Keywords: Soilphosphorus;PSM;Psolubilization;Biodiversity;Biofertilizers Introduction Phosphorusisthemostimportantkeyelementinthe nutritionofplants,nexttonitrogen(N).Itplaysanim- portantroleinvirtuallyallmajormetabolicprocessesin plantincludingphotosynthesis,energytransfer,signal transduction,macromolecularbiosynthesisandrespir- ation(Khanetal.2010)andnitrogenfixationinlegumes (Saberetal.2005).AlthoughPisabundantinsoilsin bothinorganicandorganicforms,itisamajorlimiting factorforplantgrowthasitisinanunavailableformfor rootuptake.InorganicPoccursinsoil,mostlyininsol- ublemineralcomplexes,someofthemappearingafter frequentapplicationofchemicalfertilizers.Theseinsol- uble,precipitatedformscannotbeabsorbedbyplants (RengelandMarschner2005).Organicmatterisalsoan importantreservoirofimmobilizedPthataccountsfor 20 80%ofPinsoils(Richardson1994).Only0.1%of thetotalPexistsinasolubleformavailableforplantup- take(Zhouetal.1992)becauseofitsfixationintoanun- availableformduetoPfixation.ThetermPfixationis *Correspondence: seemabhargavsharma@gmail.com 1 DepartmentofEarthandEnvironmentalScience,KSKVKachchhUniversity, MundraRoad,Bhuj370001,Gujarat,India Fulllistofauthorinformationisavailableattheendofthearticle a SpringerOpen Journal ©2013Sharmaetal.;licenseeSpringer.ThisisanopenaccessarticledistributedunderthetermsoftheCreativeCommons AttributionLicense(http://creativecommons.org/licenses/by/2.0),whichpermitsunrestricteduse,distribution,andreproduction inanymedium,providedtheoriginalworkisproperlycited. Sharma etal.SpringerPlus 2013, 2 :587 http://www.springerplus.com/content/2/1/587 usedtodescribereactionsthatremoveavailablephos-phatefromthesoilsolutionintothesoilsolidphase(Barber1995).Therearetwotypesofreactions(a)phos-phatesorptiononthesurfaceofsoilmineralsand(b)phosphateprecipitationbyfreeAlandFeinthesoilsolution(Havlinetal.1999).Thesoilsthatexhibithigh-estPfixationcapacityoccupy1,018millionhectares(ha)inthetropics(SanchezandLogan1992).ItisforthisreasonthatsoilPbecomesfixedandavailablePlevelshavetobesupplementedonmostagriculturalsoilsbyaddingchemicalPfertilizers,whichnotonlyrepresentamajorcostofagriculturalproductionbutalsoimposeadverseenvironmentalimpactsonoverallsoilhealthanddegradationofterrestrial,freshwaterandmarineresources(Tilmanetal.2001).Thus,increasedPlevelshavebeenidentifiedasamainfactorforeutrophica-tionofsurfacewatersthatmayleadtoalgalblooms(Schindleretal.2008).Therepeatedandinjudiciousappli-cationsofchemicalPfertilizers,leadstothelossofsoilfertility(Gyaneshwaretal.2002)bydisturbingmicrobialdiversity,andconsequentlyreducingyieldofcrops.Thelong-termeffectofdifferentsourcesofphosphatefertilizersonmicrobialactivitiesincludesinhibitionofsubstrate-inducedrespirationbystreptomycinsulphate(fungalactivity)andactidione(bacterialactivity)andmicrobialbiomasscarbon(C)(Bolanetal.1996).Similarly,theapplicationoftriplesuperphosphate(94kg/ha)hasshownasubstantialreductioninmicrobialrespirationandmetabolicquotient(qCO)(ChandiniandDennis2002).MoreovertheefficiencyofappliedPfertilizersinchemicalformrarelyexceeds30%duetoitsfixation,eitherintheformofiron/aluminiumphosphateinacidicsoils(NorrishandRosser1983)orintheformofcalciumphos-phateinneutraltoalkalinesoils(Lindsayetal.1989).IthasbeensuggestedthattheaccumulatedPinagriculturalsoilswouldbesufficienttosustainmaximumcropyieldsworldwideforabout100yearsifitwereavailable(Khanetal.2009a,b,c).AmajorcharacteristicofPbiogeochemistryisthatonly1%ofthetotalsoilP4,000kgP/hainthetop30cm)isincorporatedintolivingplantbiomassduringeachgrowingseason(1030kgP/ha),reflectingitslowavailabilityforplantup-take(Blakeetal.2000;QuiquampoixandMousain2005).FurthermorePisafiniteresourceandbasedonitscurrentrateofuse,ithasbeenestimatedthattheworldsknownreservesofhighqualityrockPmaybedepletedwithinthecurrentcentury(Cordelletal.2009).BeyondthistimetheproductionofPbasedfertilizerswillrequiretheprocessingoflowergraderockatsignificantlyhighercost(Isherwood2000).TherealizationofallthesepotentialproblemsassociatedwithchemicalPfertilizerstogetherwiththeenormouscostinvolvedintheirmanufacture,hasledtothesearchforenvironmentalcompatibleandeco-nomicallyfeasiblealternativestrategiesforimprovingcropproductioninloworP-deficientsoils(Zaidietal.2009).Theuseofmicrobialinoculants(biofertilisers)possesingP-solubilizingactivitiesinagriculturalsoilsisconsideredasanenvironmental-friendlyalternativetofurtherap-plicationsofchemicalbasedPfertilizers.ConstraintsinusingphosphatefertilizersThereisglobalconcernabouttheenergyandcostsin-volvedinminingtherockphosphateanditstransportfrommanufacturingsitestofarmcropfields.MiningphosphatemineralsandspreadingPfertilizersoverthelandscapeisneithereco-friendly,economicallyfeasiblenoritissustainableanditposesfollowingconstraints(i)emissionofthefluorineasthehighlyvolatileandpoison-ousHFgas,(ii)disposalofgypsumand(iii)accumulationofCdandotherheavymetalsinsoilandpossiblycropsasaresultofrepetitiveuseofPfertilizers.Atpresentminingrate(about7,100milliontones/annum),reservewillbedepletedinabout500600years.InIndia,depositsofsufficientlyenrichedphosphaticrocksarelimitedandhenceitimports2milliontonsofrockphosphateannually.About98%ofcroplandinIndiaisde-ficientinavailableformsofsoilphosphorusandonly1-9%hashighphosphorusstatus.Intensivecroppingpatternduringthisgreenandwhiterevolutionhasalsoresultedinwidespreaddeficiencyofphosphorus.AlthoughvariousamendmentsareavailableformanagementofPindifferentsoil,allarecostlierandpracticallydifficult.Thus,evenifthetotalsoilPishighandalsoifPfertilizersareappliedregularly,pHdependentchemicalfixationdeterminesthequantityofavailableP.TheholisticPmanagementinvolvesaseriesofstrategiesinvolvingmanipulationofsoilandrhizosphereprocesses,developmentofPefficientcropsandimprovingPrecyclingefficiency.MicrobialmediatedPmanagementisanecofriedlyandcosteffectiveapproachforsustainabledevelopmentofagriculturalcrop.MicroorganismsareanintegralcomponentofthesoilPcycleandareimportantforthetransferofPbetweendif-ferentpoolsofsoilP.PhosphateSolubilzingMicroorganisms(PSM)throughvariousmechanismsofsolubilizationandmineralisationareabletoconvertinorganicandorganicsoilPrespectively(Khanetal.2009a)intothebioavailableformfacilitatinguptakebyplantroots.ItisimportanttodeterminetheactualmechanismofPsolubilisationbyPSMforoptimalutilizationofthesemicroorganismsinvariedfieldconditions.Henceitisimperativetobetterunderstandtheplant-soil-microbialPcyclewiththeaimofreducingrelianceonchemicalPfertilizers.ThishasledtoincreasedinterestintheharnessingofmicroorganismstosupportPcyclinginagroecosystems.OccurrenceandisolationofPSMSolubilizationofinsolublePbymicroorganismswasre-portedbyPikovskaya(1948).Duringthelasttwodecadesetal.SpringerPlusPage2of14http://www.springerplus.com/content/2/1/587 knowledgeonphosphatesolubilizingmicroorganismsincreasedsignificantly(Richardson2001;RodriguezandFraga1999).Severalstrainsofbacterialandfungalspecieshavebeendescribedandinvestigatedindetailfortheirphosphate-solubilizingcapabilities(Glick1995;Heetal.1997).TypicallysuchmicroorganismshavebeenisolatedusingculturalprocedureswithspeciesofPseudomonasBacillusbacteria(IllmerandSchinner1992)andAspergillusfungibeingpredominant(Wakelinetal.2004).Theseorganismsareubiquitousbutvaryindensityandmineralphosphatesolubilizing(mps)abilityfromsoiltosoilorfromoneproductionsystemtoanother.InsoilPsolubilizingbacteriaconstitute1-50%andfungi0.1-0.5%ofthetotalrespectivepopulation.Theyaregenerallyisolatedfromrhizosphereandnonrhi-zospheresoils,rhizoplane,phyllosphere,androckPdepositareasoilandevenfromstressedsoilsusingserialplatedilutionmethodorbyenrichmentculturetechnique(Zaidietal.2009).Theconcentrationofironore,temperature,andCandNsourcesgreatlyinfluencetheP-solubilizingpotentialsofthesemicrobes.Amongthevariousnutrientsusedbythesemicroorganisms,ammoniumsaltshasbeenfoundtobethebestNsourcefollowedbyasparagine,sodiumnitrate,potassiumnitrate,ureaandcalciumnitrate(Ahujaetal.2007).Since1948,whenPikovskayasug-gestedthatmicrobescoulddissolvenon-readilyavailableformsofsoilPandplayanimportantroleinprovidingPtoplants,numerousmethodsandmedia,suchasPikovskaya(Pikovskaya1948),bromophenolbluedyemethod(Guptaetal.1994)andNationalBotanicalResearchInstituteP(NBRIP)medium(Nautiyal1999)havebeenproposed.ThesourceofinsolublephosphateintheculturemediatoisolatePSMisamajorissueofcon-troversyregardingtheisolationofPSMintruesense.Commonlyusedselectionfactorforthistrait,tricalciumphosphate(TCP),isrelativelyweakandunreliableasauni-versalselectionfactorforisolatingandtestingphosphate-solubilizingmicroorganisms(PSM)forenhancingplantgrowth.TheuseofTCPusuallyyieldsmany(uptoseveralthousandperstudy)isolatesofsupposedPSM.Whentheseisolatesarefurthertestedfordirectcontributionofphosphorustotheplants,onlyaveryfewaretruePSM.Othercompoundsarealsotested,butonaverysmallscale.Thesephosphates,mainlyiron/aluminiumphosphateandseveralcalciumphosphatesareevenlesssolublethanTCPinwater.BecausesoilsgreatlyvaryinpHandseveralchem-icalproperties,itappearsthatthereisnometal-PhosphatecompoundthatcanserveastheuniversalselectionfactorforPSM.Heremultiplesourcesofinsolublephosphatearerecommended.Theselectionofthemetal-PhosphatecandidatesforpotentialPSMwilldependonthetypeofsoil(alkaline,acidic,ororganic-rich)wherethePSMwillbeused.Addingcalciumphosphatecompounds(includingrockphosphates)foralkalinesoils,iron/aluminiumphosphatecompoundsforacidicsoils,andphytatesforsoilsrichinorganicPissuggestedBashanetal.2013a,b.BothbacterialandfungalstrainsexhibitingPsolubilizingactivityaredetectedbytheformationofclearhalo(asignofsolubilization)aroundtheircolonies.ProductionofahaloonasolidagarmediumshouldnotbeconsideredthesoletestforPsolubilization.Whencoloniesgrowwith-outahaloafterseveralreplacementsofthemedium,anadditionaltestinliquidmediatoassayPdissolutionshouldbeperformedandthefewisolatesthatareobtainedaftersuchrigorousselectionshouldbefurthertestedforabundantproductionoforganicacidsandtheisolatescomplyingwiththesecriteriashouldbetestedonamodelplantastheultimatetestforpotentialPsolubilization(Bashanetal.2013a).TheviablemicrobialpreparationspossessingP-solubilizingactivityaregenerallytermedasmicrophos(Zaidietal.2009).Thephosphate-solubilizingmicrobesshowinggreatersolubilization(bothqualitativelyandquantitatively)ofinsolublePunderinvitroconditionsareselectedforfieldtrialspriortoproductioninbulkforultimatetransmissionasabiofertiliser.Onceapotentialisolateisidentified,itmustbefurthertestedfordirectcontributiontoPplantnutritionandnotnecessarilytogeneralgrowthpromotion,ascom-monlydonebecausepromotionofgrowth,evenbyPSB,canbetheoutcomeofothermechanisms.(Bashanetal.2013a)andabiltytosolubilisePisnotnecessarilycorre-latedwiththeabilitytopromoteplantgrowth(Collavinoetal.2010).Theproductionofbiofertilizeranditsacceptancebyfarmingcommunitiesarecloselylinked.Foruptakebyfarmers,qualitymanagementisessentialandmustbeperformedconsistentlyinordertosupplyreliableandcontaminant-freebioproducts.Asfarasinvitrotrialsareconcernedtheestablishmentandperform-anceofthesePSMinoculatedevelopedinlaboratoryislargelyhamperedbyenvironmentalvariablesincludingsalinity,pH,moisture,temperatureandclimaticcondi-tionsofthesoil.Moreoveritisalsoknownthatinoculadevelopedfromaparticularsoilfailtofunctionasef-fectivelyinsoilshavingdifferentproperties(RodriguezandFraga1999).HencethereisaneedtostudyPSMactivityincorrelationwiththesefactorsbeforePSMapplicationasabiofertiliser.ProtocolforisolationandeffectiveinoculantsdevelopmentofPSMbasedbiofer-tiliserhasbeenshowninFigure1.BiodiversityofPsolubilizersAsubstantialnumberofmicrobialspeciesexhibitPsolubilizationcapacity;theseincludebacteria,fungi,actino-mycetesandevenalgae.InadditiontoPseudomonasBacillus,otherbacteriareportedasP-solubilizersincludeetal.SpringerPlusPage3of14http://www.springerplus.com/content/2/1/587 RhodococcusArthrobacter,Serratia,Chryseobacterium,Gordonia,Phyllobacterium,Delftiasp.(Wanietal.2005;Chenetal.2006),Azotobacter(Kumaretal.2001),Xanthomonas(DeFreitasetal.1997),Enterobacter,Pantoea,andKlebsiella(Chungetal.2005),Vibrioproteolyticus,Xanthobacteragilis(Vazquezetal.2000).Furthermore,symbioticnitrogenous,whichfixatmosphericnitrogenintoammoniaandexportthefixednitrogentothehostplants,havealsoshownPSactivity(Zaidietal.2009)Forinstance,Rhizobiumleguminosarumbv.Trifolii(Abriletal.2007),andspeciesnodulatingCrotalariaspecies(Sridevietal.2007)improvedplantP-nutritionbymobilizinginorganicandorganicP.VariousPSbacteriahavealsobeenisolatedfromstressedenviron-mentsforexamplethehalophilicbacteriaKushneriasinocarniisolatedfromthesedimentofDaqiaosalternontheeasterncoastofChina,whichmaybeusefulinsaltaffectedagriculturalsoils(Zhuetal.2011).Insoil,P-solubilizingfungiconstituteabout0.1oftotalfungalpopulations(Kucey1983).Moreover,P-solubilizingfungidonotlosethePdissolvingac-tivityuponrepeatedsubculturingunderlaboratoryconditionsasoccurswiththeP-solubilizingbacteria(Sperber1958a,b;Kucey1983).Moreover,fungiinsoilsareabletotraverselongdistancesmoreeasilythanbacteriaandhence,maybemoreimportanttoPsolubilizationinsoils(Kucey1983).Generally,theP-solubilizingfungiproducemoreacidsthanbacteriaandconsequentlyexhibitgreaterP-solubilizingactivity(Venkateswarluetal.1984).Amongfilamentousfungithatsolubilizephosphate,thegeneraAspergillusand(Feniceetal.2000;KhanandKhan2002;Reyesetal.1999,2002)arethemostrepresentativealthoughstrainsofTrichoderma(Altomareetal.1999)andRhizoctoniasolani(Jacobsetal.2002)havealsobeenreportedasPsolubilizers.AnematofungusArthrobotrysoligosporaalsohastheabilitytosolubilizephosphateinvivoaswellasinvitro(Duponnoisetal2006).Amongtheyeasts,onlyafewstud-ieshavebeenconductedtoassesstheirabilitytosolubilizephosphatetheseincludeYarrowialipolytica(Vassilevetal.2001),SchizosaccharomycespombePichiafermentansAsmorestudiesareconducted,awiderdiversityofphosphate-solubilizingfilamentousfungiareexpectedtobedescribed.Ofthoseidentified,manyarecommonlyfoundinagriculturalsoilssuchasPenicilliumsp.Mucorsp.andAspergillussp.whichhasbeenshowntoincreaseplantgrowthby520%afterinoculation(Gunesetal.2009).TheP-solubilizingabilityofactinomyceteshasattractedinterestinrecentyearsbecausethisgroupofsoilorganismsisnotonlycapableofsurvivinginextremeenvironments(e.g.drought,fire.)butalsopossessotherpotentialbenefits(e.g.productionofantibioticsandphytohormone-likecompounds)thatcouldsimultaneouslybenefitplantgrowth(Fabreetal.1988;Hamdalietal.2008a,b).AstudybyHamdalietal.(2008a)hasindicatedthatapproximately20%ofactinomycetescansolubilizeP,includingthoseinthecommongeneraStreptomycesMicromonosporaApartiallistofPSMincludingvariousgroupsisgiveninTable1.Inadditiontobacteria,fungiandactinomycetes,algaesuchascyanobacteriaandmycorrhizahavealsobeenreportedtoshowPsolubilizationactivity.Theinter-activeeffectsofarbuscularmycorrhizalfungi(AMF)andrhizobacteriaonthegrowthandnutrientsuptakeofSorghumbicolorwerestudiedinacidandlowavailabil-ityphosphatesoil.ThemicrobialinoculaconsistedoftheAMFsGlomusmanihotisandEntrophosporacolombianaPSBPseudomonassp.,resultsindicatedthattheinter-actionofAMFandtheselectedrhizobacteriahasapo-tentialtobedevelopedasbiofertilizersinacidsoil.ThepotentialofdualinoculationwithAMFandrhizobac-terianeedstobefurtherevaluatedunderdifferentcropandagroclimaticconditions,particularlyinthefield(Widadaetal.2007). Serial dilutionInoculation on media (pour plate/streaking) having different sources of insoluble P,depending on soil typeClear zone around colony growth indicates PSM activityAdditional test in liquid media to assay P dissolutionTest isolates for abundant production of organic acidsPure cultures by reinoculationStudy of the morphology and colony characteristics and biochemical testsScreening of best inoculants in terms of P solubilizing activityIdentification at genetic level (molecular characterization)Test on a model plantDevelopment of microphosGreen house trialsField trialsStandardization (quality control)Commercial biofertiliser Figure1ProtocolforisolationanddevelopmentofeffectiveinoculantsofPSMbasedbiofertiliser.etal.SpringerPlusPage4of14http://www.springerplus.com/content/2/1/587 Hencethestudieshaveshownthatthediversityofthesishighlyvariedindifferentecologicalnichesandthereisamplescopetoidentifymanynewpotentiso-latesfromvariedenvironmentsincomingtimes.MechanismofP-solubilizationbyPSMInareviewofPchemistryinsoils,SimsandPierzynski(2005)identifiedthemajorprocessesofthesoilPcyclethataffectsoilsolutionPconcentrationsas(1)dissol-precipitation(mineralequilibria),(2)sorptiondesorption(interactionsbetweenPinsolutionandsoilsolidsurfaces),and(3)mineralizationimmobilization(biologicallymediatedconversionsofPbetweeninorganicandorganicforms).ThemainPsolubilizationmechanismsemployedbysoilmicroorganismsinclude:(1)releaseofcomplexingormineraldissolvingcompoundse.g.organicacidanions,siderophores,protons,hydroxylions,CO,(2)liberationofextracellularenzymes(biochemicalPmineralization)and(3)thereleaseofPduringsubstratedegradation(biologicalPmineralization)(McGillandCole1981).Therefore,microorganismsplayanimportantroleinallthreemajorcomponentsofthesoilPcycle(i.e.dissolutionprecipitation,sorptiondesorption,andmineralizationimmobilization).AdditionallythesemicroorganismsinthepresenceoflabileCserveasasinkforP,byrapidlyimmo-bilizingiteveninlowPsoils;thereforePSMbecomeasourceofPtoplantsuponitsreleasefromtheircells.ReleaseofPimmobilizedbyPSMprimarilyoccurswhencellsdieduetochangesinenvironmentalconditions,star-vationorpredation.Environmentalchanges,suchasdry-rewettingorfreezingthawing,canresultinso-calledflush-events,asuddenincreaseinavailablePinthesolutionduetoanunusuallyhighproportionofmicrobialcelllysis(Butterlyetal.2009).(Griersonetal.1998)foundthatabout3045%ofmicrobialP(0.81mgkg)wasreleasedinasandyspodosolinaninitialflushafterdryingrewettingcycleswithinthefirst24hour.A)InorganicPsolubilization:byP-solubilizingmicroor-ganismsoccursmainlybyorganicacidproduction(Table2),eitherby:(i)loweringthepH,or(ii)byenhancingchelationofthecationsboundtoP(iii)bycompetingwithPforad-sorptionsitesonthesoil(iv)byformingsolublecomplexeswithmetalionsassociatedwithinsolubleP(Ca,Al,Fe)andthusPisreleased.TheloweringinpHofthemediumsuggeststhereleaseoforganicacidsbytheP-solubilizingmicroorganisms(Whitelaw2000;Malihaetal.2004)viathedirectoxidationpathwaythatoccursontheouterfaceofthecytoplasmicmembrane(Zaidietal.2009).Theseacidsaretheproductofthemicrobialmetabolism,mostlybyoxidativerespirationorbyfermentationofor-ganiccarbonsources(e.g.,glucose)(AtlasandBartha1997;Troloveetal.2003)orsuchorganicacidscaneitherdirectlydissolvethemineralPasaresultofanionexchangeofphosphatebyacidanionorcanchelateFe,AlandCaionsassociatedwithP(Omar1998).ThemonovalentanionphosphateHisamajorsolubleformofinorganicphosphate,whichusuallyoccursatlowerpH.HoweverasthepHofthesoilen-vironmentincreasesthedivalentandtrivalentformsofPi(HPOandHPOrespectively)occur.Thus,thesynthesisanddischargeoforganicacidbythePSMstrainsintothesurroundingenvironmentacidifythecellsandtheirsurroundingenvironmentthatultim-atelyleadtothereleaseofPionsfromthePmineralbyHsubstitutionforthecationboundtophosphate(Goldstein1994).TheprominentacidsreleasedbyPSMinthesolubilizationofinsolubleParegluconicacid(Di-Simineetal.1998;Bar-Yosefetal.1999),oxalicacid,citricacid(Kimetal.1997),lacticacid,tartaricacid,aspar-ticacid(Venkateswarluetal.1984).EvidencefromanabioticstudyusingHClandgluconicacidtosolubilizePalsoindicatedthatchelationofAlbygluconicacidmayhavebeenafactorinthesolubilizationofcolloidalAlphosphate(Whitelawetal.1999).OrganicacidsproducedbyP-solubilizingmicroorganismscanbedetected Table1BiodiversityofPSMAlcaligenessp.,Aerobactoraerogenes,Achromobactersp.,Actinomaduraoligospora,Agrobacteriumsp.,Azospirillumbrasilense,Bacillussp.,Bacilluscirculans,B.cereus,B.fusiformis,B.pumils,B.megaterium,B.mycoides,B.polymyxa,B.coagulansB,.chitinolyticus,B.subtilis,Bradyrhizobiumsp.,Brevibacteriumsp.,Citrobactersp.,Pseudomonassp.,Pputida,P.striata,P.fluorescens,P.calcis,Flavobacteriumsp.,Nitrosomonassp.,Erwiniasp.,Micrococcussp.,Escherichiaintermedia,Enterobacterasburiae,Serratiaphosphoticum,Nitrobactersp.,Thiobacillusferroxidans,T.thioxidans,Rhizobiummeliloti,Xanthomonassp.Aspergillusawamori,A.niger,A.tereus,A.flavus,A.nidulans,A.foetidus,A.wentii.Fusariumoxysporum,Alternariateneius,Achrothciumsp.Penicilliumdigitatum,Plilacinium,Pbalaji,P.funicolosum,Cephalosporiumsp.Cladospriumsp.,Curvularialunata,Cunnighamella,Candidasp.,Chaetomiumglobosum,Humicolainslens,Humicolalanuginosa,Helminthosporiumsp.,Paecilomycesfusisporous,Pythiumsp.,Phomasp.,Populosporamytilina,Myrotheciumroridum,Morteirellasp.,Micromonosporasp.,Oideodendronsp.,Rhizoctoniasolani,Rhizopussp.,Mucorsp.,Trichodermaviridae,Torulathermophila,Schwanniomycesoccidentalis,Sclerotiumrolfsii.ActinomycetesActinomyces,,Streptomyces.CyanobacteriaAnabenasp.,Calothrixbraunii,Nostocsp.,Scytonemasp.,Glomusfasciculatum.etal.SpringerPlusPage5of14http://www.springerplus.com/content/2/1/587 byhighperformanceliquidchromatographyandenzymaticmethods(Parksetal.1990;Whitelaw2000).However,acidificationdoesnotseemtobetheonlymechanismofsolubilization,astheabilitytoreducethepHinsomecasesdidnotcorrelatewiththeabilitytosolubilizemineralP(SubbaRao1982).Altomareetal.(1999)investigatedthecapabilityoftheplant-growthpromotingandbiocontrolT.harzianumT-22tosolubilizeinvitroinsolublemineralsincludingrockphosphate.Organicacidswerenotdetectedintheculturefiltratesandhence,theauthorsconcludedthatacidificationwasprobablynotthemajormechanismofsolubilizationasthepHneverfellbelow5.Thephosphatesolubilizingactivitywasattributedbothtochelationandtoreductionprocesses.Although,organicacidhasbeensuggestedastheprincipalmechanismofPsolubilization,thesolubilizationofinsolublePbyinorganic(e.g.HCl)hasalsobeenreported,althoughHClwasabletosolubilizelessPfromhydroxyapatitethancitricacidoroxalicacidatsamepH(Kimetal.1997).BacteriaofthegeneraNitrosomonasThiobacillusspeciescanalsodissolvephosphatecompoundsbyproducingnitricandsulphuricacids(AzamandMemon1996).Accordingtothesinktheory,P-solubilizingorgan-ismsremoveandassimilatePfromtheliquidhence,activatetheindirectdissolutionofcalciumphos-phatecompoundsbyconsistentremovalofPfromliquid Table2ImportantPSM,theirecologicalnichesandorganicacidsproducedOrganismEcologicalnichePredominantacidsproducedReferencePSBSoilandphosphatebearingrocksND(notdetermined)PikovskayaPSBBulkandrhizosphericsoilND(notdetermined)GerretsonEscherichiafreundiiSoilLacticSperberAspergillusniger,Penicilliumsp.SoilCitric,glycolic,succinic,gluconic,oxalic,lacticBacillusmegaterium,Pseudomonassp.,BacillussubtilusRhizosphericsoilLactic,malicTahaetal.Arthrobactersp.,Bascillussp.,BacillusfirmusB-7650WheatandcowpearhizosphereLactic,citricBajpaiandSundaraRao1971Aspergillussp.,Penicilliumsp.,ChaetomiumnigricolorLateriticsoilOxalic,Succinic,Citric,2-ketogluconicBanikandDeyA.japonicus,A.foetidusIndianRockphosphateOxalic,citric,gluconicsuccinic,tartaricacidSingaletal.P.radicumrhizosphereofwheatroots,GluconicWhitelawetal.EnterobacteragglomeransWheatrhizosphereOxalic,citricKimetal.Bacillusamyloliquefaciens,B.licheniformis,B.atrophaeus,Penibacillusmacerans,Vibrioproteolyticus,xanthobacteragilis,Enterobacteraerogenes,E.taylorae,E.asburiae,Kluyveracryocrescens,Pseudomonasaerogenes,ChryseomonasLuteolaMangroveecosystemLactic,itaconic,isovaleric,isobutyric,aceticVazquezetal.PenicilliumrugulosumVenezuelanphosphaterocksCitric,gluconicacidReyesetal.EnterobacterintermediumGrassrhizosphere2-ketogluconicHwangboetal.Aspergillusflavus,A.niger,PenicilliumcanescensstoredwheatgrainsOxalic,citric,gluconicsuccinicMalihaetal.RootfragmentsandrhizosphereofoilpalmtreesCitric,malic,tartaric,gluconicFankemetal.AspergillusnigerTropicalandsubtropicalsoilGluconic,oxalicChuangetal.rhizosphereofHippophaerhamnoidesgrowinginthecolddesertsofLahaulandSpitiinthetrans-HimalayasLactic,formicVyasandGulatiB.pumilusvar.2;B.subtilisvar.2;Actinomaduraoligospora;Citrobactersp.GiantCardoncactus(P.pringlei)growinginancientlavaGluconic,Propionic,Isovaleric,Heptonic,Caproic,Isocaproic,Formic,Valeric,Succinic,Oxalic,Oxalacetic,Malonic.Puenteetal.B.pumilusCHOO8A;B.fusiformisChollacactus(OpuntiaCholla)Puenteetal.Bacillussp.SENDO6andGiantCardoncactus(P.pringlei)Gluconic,Propionic,Isovaleric,Formic,Succinic,Lactic.Puenteetal.PseudomonasputidaM5TSA,EnterobactersakazakiiM2PFe,andBacillusmegateriumM1PCaWildcactusMammillariafraileanaLopezetal.etal.SpringerPlusPage6of14http://www.springerplus.com/content/2/1/587 culturemedium.Forinstance,thePcontentinthebiomassPseudomonassp.andP.aurantiogriseumweresimilartothoseobservedinnon-P-solubilizingmicroorganisms(Illmeretal.1995)whichcanbeexplainedbythefactthatthePcontentinbiomassoforganismsisconsistentlycorrelatedwiththedecompositionofPcontainingorganicsubstrates(DightonandBoddy1989).TheothermechanismistheproductionofHwhichreactwithferricphosphatetoyieldferroussulphatewithconcomitantreleaseofphosphate(SwabyandSperber1958).IthasbeensuggestedthatMPSactivityoccursasacon-sequenceofmicrobialsulphuroxidation(Rudolph1922),nitrateproductionandCOformation.Theseprocessesresultintheformationofinorganicacidslikesulphuricacid(Sperber1958a).However,theireffectivenesshasbeenlessacceptedthantheconceptofinvolvementoforganicacidsinsolubilization(Kimetal.1997).excretionoriginatingfromNHassimilationproposedbyParksetal.(1990)couldbethealternativemechanismsofPsolubilization.AnHPLCanalysisoftheculturesolutionofPseudomonassp.,incontrasttotheexpectation,didnotdetectanyorganicacidwhilesolubilizationoccurred(IllmerandSchinner1995).TheyalsoreportedthatthemostprobablereasonforsolubilizationwithoutacidproductionisthereleaseofprotonsaccompanyingrespirationorNHassimilation.Krishnarajetal.(1998)haveproposedamodelhighlight-ingtheimportanceofprotonsthatarepumpedoutofthecelltobethemajorfactorresponsibleforPsolubilization.Heredirectroleoforganicorinorganicacidshasbeenruledout.Forsomemicroorganisms,NHdrivenpro-tonreleaseseemstobethesolemechanismtopromotePsolubilization.Aseaetal.(1988)testedtwofungi,PenicilliumbilaiiPenicilliumfuscum,fortheirabilitytosolubilizephosphaterockinthepresenceoforwithoutNaddition,andshowedthatonlyP.bilaiimaintainedtheabilitytodecreasethepHandmobilizePwhennoNwassupplied.InastudyofPseudomonasfluorescens,theformofCsupply(e.g.glucoseversusfructose)ratherthanNsupply(e.g.NHversusNO)hadthegreatesteffectonprotonrelease(Parketal.2009).Further,theinvolvementoftheHpumpmechanisminthesolubilizationofsmallamountsofPinPenicilliumrugulosumisreported(Reyesetal.1999).Acidificationoftherhizosphereofcactusseedlings(giantcardon,Pachycereuspringlei)afterinoculationwiththeplantgrowth-promotingbacteriumAzospirillumbrasilenseinthepresenceorabsenceofammoniumandnitrate,wasstudiedanditwasassumedthattheeffectofin-oculationwiththisPGPBonplantgrowth,combinedwithnitrogennutrition,mightbeaffectingoneormoreofthemetabolicpathwaysoftheplantwhichincreasesprotoneffluxfromrootsandliberationoforganicacid,leadingtorhizosphereacidification(Carrilloetal.2002).Thisindicatesthatfordifferentspecies,differentmechanismsareresponsibleforprotonrelease,onlypartlydependingonthepresenceofNHGoldstein(1995)suggestedthatextracellularoxidationviadirectoxidationpathwaymayplayanessentialroleinsoilswherecalciumphosphatesprovideasignificantpoolofunavailablemineralphosphorus.Thishasbeenconfirmedbysomeresearchers(Songetal.2008)bybiochemicalanalysisofloweringofpHininsolublePsolubilizationbyBurkholderiacepaciaDA23.B)OrganicPsolubilizationisalsocalledmineralizationoforganicphosphorus.MineralizationofsoilorganicP(Po)playsanimperativeroleinphosphoruscyclingofafarmingsystem.OrganicPmayconstitute4ofthetotalsoilP(Khanetal.2009b).SuchPcanbereleasedfromorganiccompoundsinsoilbyenzymes:Non-specificacidphosphatases(NSAPs),whichdephosphorylatephospho-esterorphosphoanhydridebondsoforganicmatter.AmongthevarietyofphosphataseenzymeclassesreleasedbyPSM,phosphomonoesterases(oftenjustcalledphosphatases)arethemostabundantandbeststudied(Nannipierietal.2011).DependingontheirpHoptima,theseenzymesaredividedintoacidandalkalinephosphomonoesterasesandbothcanbeproducedbyPSMdependingupontheexternalconditions(Kimetal.1998;Jorqueraetal.2008Typically,acidphosphatasespredominateinacidsoils,whereasalkalinephosphatasesaremoreabundantinneutralandalkalinesoils(EivaziandTabatabai1977JumaandTabatabai19771998;Renellaetal.2006Althoughplantrootscanproduceacidphosphatasestheyrarelyproducelargequantitiesofalkalinephosphatases,suggestingthatthisisapotentialnicheforPSM(JumaandTabatabai1998;Criquetetal.2004).Itisalsodifficulttodifferentiatebetweenroot-andPSM-producedphosphatases(Richardsonetal.2009a)butsomeevidencesuggeststhatphosphatasesofmicrobialoriginpossessagreateraffinityforPocompoundsthanthosederivedfromplantroots(Tarafdaretal.2001).TherelationshipbetweenPSMintroducedintosoil,phosphataseactivityandthesubsequentmineralizationofPostillremainspoorlyunderstood(Chenetal.2003phytases,whichspecificallycausereleaseofPfromphytatedegradation.Initsbasicform,phytateistheprimarysourceofinositolandthemajorstoredformofPinplantseedsandpollen,andisamajorcomponentoforganicPinsoil(Richardson,1994AlthoughtheabilityofplantstoobtainPdirectlyfromphytateisverylimited,yetthegrowthandP-nutritionofArabidopsisplantssuppliedwithetal.SpringerPlusPage7of14http://www.springerplus.com/content/2/1/587 phytatewassignificantlyimprovedwhentheyweregeneticallytransformedwiththephytasegene(phyA)derivedfromAspergillusniger(Richardsonetal.2001).ThisledtoanincreaseinP-nutritiontosuchanextentthatthegrowthandP-contentoftheplantwasequivalenttocontrolplantssuppliedwithinorganicP.HencemicroorganismsareinfactakeydriverinregulatingthemineralizationofphytateinsoilandtheirpresencewithintherhizospheremaycompensateforaplantsinabilitytootherwiseacquirePdirectlyfromphytate(RichardsonandSimpson2011phosphonatasesandCPlyases,thatcleavetheCbondoforganophosphonates(Rodriguezetal.2006ItisthereforeclearthatPsolubilizationbyPSMshasbeenasubjectofanalysisandresearchforalongtimeandstilltheresearchseemstobeinitsinfancy.Itoccursthroughdifferentmechanismsandthereisconsiderablevariationamongsttheorganismsinthisrespect.EachorganismcanactinoneormorethanonewaytobringaboutthesolubilizationofinsolubleP.Thoughitisdif-ficulttopinpointasinglemechanism,productionoforganicacidsandconsequentpHreductionappearstobeofgreatimportance.DifferentmechanismsinvolvedinthesolubilizationandmineralizationofinsolublePbynaturally-occurringmicrobialcommunitiesofsoilsarebrieflyillustratedinFigure2.RoleofsiderophoresinPsolubilizationSiderophoresarecomplexingagentsthathaveahighaffin-ityforironandareproducedbyalmostallmicroorganismsinresponsetoirondeficiency.Thussiderophoresactassolubilizingagentsforironfrommineralsororganiccompoundsunderconditionsofironlimitation.Thereareapproximately500knownsiderophores,withthemajorityofthembeingusedbyawiderangeofmicroor-ganismsandplantsandsomeofthembeingexclusivelyusedbythemicrobialspeciesandstrainsthatproducethem(Crowley2007).StudieshavereportedthereleaseofsiderophoresfromPSM(Vassilevetal.2006;Caballero-Melladoetal.2007;Hamdalietal.2008a);however,siderophoreproductionhasnotbeenwidelyimpli-catedasaP-solubilizationmechanism.ConsideringthedominanceofmineraldissolutionoverligandexchangebyorganicacidanionsasaP-solubilizingmechanism(Parkeretal.2005),thepotentialroleofsiderophoresinenhancingPavailabilityshouldbeobvious.RoleofEPSinPsolubilizationRecentlytheroleofpolysaccharidesinthemicrobialmediatedsolubilizationofPwasassessedbyYietal.(2008).Microbialexopolysaccharides(EPSs)arepolymersconsistingmainlyofcarbohydratesexcretedbysomebac-teriaandfungiontotheoutsideoftheircellwalls.Theircompositionandstructuresareveryvaried;theymaybehomo-orheteropolysaccharidesandmayalsocontainanumberofdifferentorganicandinorganicsubstituents(Sutherland2001).FourbacterialstrainsofEnterobactersp.(EnHy-401),Arthrobactersp.(ArHy-505),Azotobactersp.(AzHy-510)andEnterobactersp.(EnHy-402),possessingtheabilitytosolubilizeTCP(tricalciumphosphate),wereusedtoassesstheroleofexopolysaccharide(EPS)inthe pool pool THROUGH ENZYMES -BLE PHOSPHO--RUS ORGANIC ACID PRODUCTION/CHELATION OF CATIONS BOUND TO PINORGANIC ACID PRODUCTIOH2S PRODUCTIONP ASSIMILATION FROM LIQUID(INDIRECT DISSOLUTION)RESPIRATORY H2CO3 PRODUCTIONPROTON RELEASE FOM NH4+ASSIMILATION/RESPIRATIONLOWERING pH THROUGH RELEASE OFPROTONSSIDEROPHORESEXOPOLYSACCHARIDESDIRECT OXIDATION PATHWAY ACID PHOSPHATASEPHYTASEPHOSPHONOTASE/ C-P LYSASE PHOSPHO--RUS Figure2SchematicrepresentationofmechanismofsoilPsolubilization/mineralizationandimmobilizationbyPSM.etal.SpringerPlusPage8of14http://www.springerplus.com/content/2/1/587 solubilizationofPbyYietal.2008.ThesePhosphateSolu-bilizingbacteriaproducedasignificantamountofEPSanddemonstratedastrongabilityforP-solubilization.HoweverfurtherstudiesarenecessarytounderstandtherelationshipbetweenEPSproductionandphosphatesolubilization.PlantgrowthpromotingattributesofPSMBesidesmakingsolublePaccessibleforuptakebyplants,therehavebeenanumberofreportsonplantgrowthpro-motionbythesemicroorganisms(GaurandOstwal1972).Thisisachievedbyproductionofplantbeneficialmetabo-lites,suchasphytohormones,antibiotics,orsiderophores.VariousPSMpreparationshavebeenshowntopromotethegrowthofmanycrops(Table3).EndophyticBacteriaisolatedfromrhizoplaneofcactigrowinginbarelavarocks,notonlysignificantlymobilizedPhosphateandotherminerals(Puenteetal.2004a,2009a)butalsopromotedgrowthofwildcactusspecies(Puenteetal.2004b,b).ThemechanismsinvolvedinplantgrowthpromotionbyPSMareoutlinedinFigure3.GeneticengineeringofPSMAlthoughknowledgeofthegeneticsofphosphatesolubilizationisstillscanty,andthestudiesatthemolecu-larlevelinordertounderstandhowpreciselythePSMbringsoutthesolubilizationofinsolublePareinconclu-sive(Rodriguezetal.2006).However,somegenesinvolvedinmineralandorganicphosphatesolubilizationhavebeenisolatedandcharacterized.Initialachievementsinthemanipulationofthesegenesthroughgeneticengineeringandmolecularbiotechnologyfollowedbytheirexpressioninselectedrhizobacterialstrainsopenapromisingperspec-tiveforobtainingPSMstrainswithenhancedphosphatesolubilizingcapacity,andthus,amoreeffectiveuseofthesemicrobesasagriculturalinoculants.TheinitialachievementincloningofgeneinvolvedinPsolubilizationfromtheGramnegativebacteriaErwiniaherbicolawasachievedbyGoldsteinandLiu(1987).SimilarlythenapAphosphatasegenefromthesoilbacteriumMorganellamorganiiwastransferredtoBurkholderiacepaciaIS-16,astrainusedasabiofertilizer,usingthebroad-hostrangevectorpRK293(Fragaetal.2001).Anincreaseinextracellularphosphataseactivityoftherecombinantstrainwasachieved.Introductionorover-expressionofgenesinvolvedinsoilphosphatesolubilization(bothorganicandinorganic)innaturalrhizospherebacteriaisaveryattractiveapproachforimprovingthecapacityofmicroorganismstoworkasinoculants.Insertionofphosphate-solubilizinggenesintomicroorganismsthatdonothavethiscapabilitymayavoidthecurrentneedofmixingtwopopulationsofbacteria,whenusedasinoculants(nitrogenfixersandphosphate-solubilizers(Bashanetal.2000).Thereareseveraladvantagesofdevelopinggenetically-modifiedPSMovertransgenicplantsforimprovingplantperformance:(1)Withcurrenttechnologies,itisfareasiertomodifyabacteriumthancomplexhigherorganisms,(2)Severalplantgrowth-promotingtraitscanbecombinedinasingleorganism,and(3)Insteadofengineeringcropbycrop,asingle,engineeredinoculantcanbeusedforseveralcrops,especiallywhenusinganon-specifcgenuslikeAzospirillum(Rodriguezetal.2006).Somebarriersshouldbeovercomefirsttoachievesuccessfulgeneinser-tionsusingthisapproach,suchasthedissimilarityofmetabolicmachineryanddifferentregulatingmechanismbetweenthedonorandrecipientstrains.Despitethediff-culties,significantprogresshasbeenmadeinobtaininggeneticallyengineeredmicroorganismsforagriculturaluse(Armarger2002).Overall,furtherstudiesonthisaspectofPSMwillprovidecrucialinformationinfutureforbetteruseofthesePSMinvariedenvironmentalconditions.CurrenttrendsPhosphorusisanimportantlimitingfactorinagricultureproduction,andconsideringthenegativeeffectsofchem-icalPfertilizers,microbialinterventionofPSMseemstobeaneffectivewaytosolvethephosphorusavailabilityinsoil.HoweverP-solubilizationinsoilismuchmoredifficulttostudythansolubilizationofPinbrothculture.ThecropsresponddifferentlytotheinoculationofPSMsandaredependentonseveralfactorssuchasthesoiltemperature,moisture,pH,salinity,andsourceofinsolubleP,methodofinoculation,theenergysourcesandthestrainofmicro-organismused.HencestudyofPSMactivityincorrelationwiththesefactorshastobedoneextensivelybeforePSMcanbeusedasabiofertiliserwithpromisingresults.Thesuccessfulimplementationofthisapproachhasalreadybeendemonstratedinthefieldsbyvariousworkers,toalimitedextent.Howeverthelargescaleuseofthistechnol-ogywouldbenefitfromadditionalstudies,particularlythosedirectedtowardsunderstandinghowtheinteractionbetweensoilandmicrobialsystemmightbefacilitated.Theorganismsinvolvedinphosphorus(P)cyclinginsoilsarehighlyvaried,andmicroorganismsprobablyplaythemostimportantrole.However,morethan99%ofsoilmicroorganismshavenotbeenculturedsuccessfully(TorsvikandOvreas2002).Therefore,culture-independentmethodsarerequiredtostudythefunctionandecologyof Table3PlantgrowthpromotionbyPSM(Patiletal.2002)PSMBioinoculantCropbenefitedB.firlmusNCIM2636PaddyinacidsoilsG.faciculatumB.megateriumG.faciculatumPhosphobacteriumSwordbeanvarietySBS1P.StriataSoybeaninsandyalluvialsoilP.StriataChickpeaetal.SpringerPlusPage9of14http://www.springerplus.com/content/2/1/587 microbesinvolvedinPcyclinginsoils.Molecularap- proachesforsuchculture-independentmethodshave beendevelopedintherecentpast.Themoleculartech- niquesbasedonnucleicacidcompositionlikeLMW RNAprofilingandPCRbasedtechniques,areexcellent toolsforthispurpose,astheyareprecise,reproducible andnotdependentonculturemediacompositionor growthphaseofmicroorganisms(Peixetal.2007). Molecular-basedtechniquesalsoprovidenewoppor- tunitytodetectthepresenceandabundanceofspecific microorganismsortoquanti fytheexpressionoftarget genesdirectlyinsoilorintherhizospherewithhigh levelsofsensitivity.Forexample,specificprimersbased onconservedregionshavebeendescribedforvarious microorganismsassociatedwithPmobilization,including mycorrhizalfungi,Penicil liumsp.,andPseudomonas sp.(Oliveiraetal.2009),ashaveprimersthataredirected attraitssuchasbacterialphytases(Jorqueraetal.2011). Microarrayscomposedofsui tesoffunctionalbacterial genesandarraysforphylogeneticanalysisofbacterial diversitybasedon16S-RNAgenesequencesalongwith next-generationsequencingandsoilmicrobiomeanalyses; providefurtherapplicationforassessmentofdiversity surroundingparticulartraitsorfunctionalgroupsofmicro- organisms(RichardsonandSimpson2011).Collectively, thesetoolsprovidenewopportunitiestoaddresskey questionsinmicrobialcommunityecologyandtoassess thesurvivalandpersistenceofspecificinoculantsunder differentenvironmentalconditions. Lookingatthepossibleavenueswhichcanopenupwith exploringtheseenvironmenta lfriendlymicroorganisms,it isnecessarytostudythecompositionanddynamicsof thesemicrobialpopulationst oreachabetterunderstanding ofsoilPSMdiversityandPuptakebyplants. Futureprospects Despitetheirdifferentecologicalnichesandmultiple functionalproperties,P-solubilizingmicroorganismshave yettofulfilltheirpromiseascommercialbio-inoculants. Currentdevelopmentsinourunderstandingofthe functionaldiversity,rhizosph erecolonizingability,modeof actionsandjudiciousapplicationarelikelytofacilitate theiruseasreliablecomponentsinthemanagementof sustainableagriculturalsystems.Althoughsignificant studiesrelatedtoPSMandtheirroleinsustainable agriculturehavebeendoneoverthelastfewdecades, therequiredtechniqueremainsinitsinfancy.Never- thelesswithanawarenessofthelimitationsofexisting methods,areassessmentcanbeexpected,sothatthe useofPSMaspotentialbiofertilisersindifferentsoil conditionsbecomesareality. EnhancementintheuseofPSMisoneofthenewly emergingoptionsformeetingagriculturalchallengesim- posedbythestill-growingdemandforfood.Thus,more thanever,obtaininghighyieldsisthemainchallengefor agriculture.Inaddition,inrecentyearsbothproducers andconsumershaveincreasinglyfocusedonthehealth andqualityoffoods,aswellasontheirorganolepticand PHOSPHATE SOLUBILIZING MICROORGANISMS PRODUCTION OF GROWTH PROMOTING SUBSTANCES SOLUBLE P ORGANIC P INORGANIC P RELEASE CONTROL AGENTS IAA ACC DEAMINASE ANTIIOXIDANTS NITROGEN FIXATION RELEASE OF TRACE ELEMENTS(Fe, Zn) GIBBERLIN CYTOKININ EXOPOLY SACCHARIDES ROOT PROLIFERATION LYTIC ENZYMES HCN SIDEROPHORES ANTIFUNGAL AGENTS ANTIBIOTICS PHENAZINES SOLUBILIZATION/ MINERALIZATION ETHYLENE MODULATION PLANT GROWTH PROMOTION UPTAKE OF HEAVY METALS OF BIO- Figure3 PossibleMechanismsinvolvedinplantgrowthpromotionbyPSM. Sharma etal.SpringerPlus 2013, 2 :587 Page10of14 http://www.springerplus.com/content/2/1/587 nutritionalproperties.Hence,thisbiotechnologyisalsolikelytoensureconservationofourenvironments.How-ever,beforePSMcancontributetosuchbenefits,scientistsmustlearnmoreaboutthemandexplorewaysandmeansfortheirbetterutilizationinthefarmersfields.Futureresearchshouldfocusonmanagingplantmicrobein-teractions,particularlywithrespecttotheirmodeofactionsandadaptabilitytoconditionsunderextremeenvironmentsforthebenefitofplants.Furthermore,scientistsneedtoaddresscertainissues,likehowtoimprovetheefficacyofbiofertilizers,whatshouldbeanidealanduniversaldeliverysystem,howtostabilizethesemicrobesinsoilsystems,andhownutritionalandrootexudationaspectscouldbecontrolledinordertogetmaximumbenefitsfromPSMapplication.BiotechnologicalandmolecularapproachescouldpossiblydevelopmoreunderstandingaboutPSMmodeofactionsthatcouldleadtomoresuccessfulplantmicrobeinteraction.EffortsshouldalsobedirectedtowardstheuseofPSMtoreducepesticideapplications.Inbrief,PSMbiotechnologyprovidesanexcellentopportunitytodevelopenvironment-friendlyphosphorusbiofertilizertobeusedassupplementsand/oralternativestochemicalfertilizers.ConclusionsPhosphorusisavitalelementincropnutrition.AdverseenvironmentaleffectsofchemicalbasedPfertilsers,depletingresourcesofhighgradePhosphaticrocksandtheirskyrocketingpriceshavecompelledustofindasustainableapproachforefficientPavailabilityinagricul-turetomeettheeverincreasingglobaldemandoffood.SoilmicroorganismsareinvolvedinarangeofprocessesthataffectPtransformationandthusinfluencethesubsequentavailabilityofP(asphosphate)toplantroots.Inparticular,microorganismscansolubilizeandmineralizePfrominorganicandorganicpoolsoftotalsoilP.TheuseofefficientPSM(phosphate-solubilizingmicroorganisms),opensupanewhorizonforbettercropproductivitybesidessustainingsoilhealth.However,theviabilityandsustainabilityofPSMtechnologylargelydependsonthedevelopmentanddistributionofgoodqualityinoculantstofarmingcommunities.Therefore,thereisaneedforextensiveandconsistentresearcheffortstoidentifyandcharacterizemorePSMwithgreateref-ficiencyfortheirultimateapplicationunderfieldcon-ditions.SoilScientistsandMicrobiologistshaveagreatresponsibilitytothesocietytofindwaysandmeansastohowsoilPcouldbeimprovedwithoutapplyingthechemicalPfertilizersunderdifferentagro-climaticregionsoftheworld.ThepromiseofexploitingsoilmicroorganismstoincreasemobilizationofsoilPremains.Whetherornotthiswillbeachievedthroughbettermanagementofsoilmicrobialcommunities,bydevelopmentofmoreeffectivemicrobialinoculants,throughthegeneticmanipula-tionofspecificorganisms,orwithacombinationoftheseapproachesisnotknown.WhatisclearthoughisthatsoilmicroorganismsplayanimportantroleinthemobilizationofsoilPandthatdetailedunderstandingoftheircontributiontothecyclingofPinsoil-plantsystemsisrequiredforthedevelopmentofsustainableagricultureandourmovementfromagreenrevolutiontoanevergreenrevolutioncanbeaccompolished.CompetinginterestsTheauthorsdeclarethattheyhavenocompetinginterests.SBS:Collectedandreviewedtheliteratureanddraftedthemanuscript.RZS:Providedguidanceandimprovedthemanuscript.MHT:providedguidance.GAT:providedguidance.Allauthorsreadandapprovedthefinalmanuscript.informationAuthorSBSisthePrincipalInvestigatorofaprojectentitledStudyofthemicrobiologicaldiversityindifferentagriculturalsoilsofkachchhwithspecialreferencetoPhosphateSolubilisingMicrobes.TheprojectisfundedbytheWomenScientistScheme(WOS-A)ofDepartmentOfScienceAndTechnology,GovernmentofIndia,NewDelhi.Underthisprojectagriculturalfieldsapplyingdifferentamendmentsarestudiedfortheirmicrobialdiversityaswellasphysicochemicalpropertiesinvariousseasonsandanycorrelationwhich,ifexistsisbeingstudied.TheinsightsgainedthroughthisstudywillhelptounderstandthemicrobialdiversityinthisveryuniqueecologicalzoneofKachchh,Gujarat,WesternIndia.AcknowledgementsFinancialsupportfromDepartmentOfScienceAndTechnology,GovernmentofIndia,NewDelhiforthefellowshipundertheWOS-A(WomenScientist-A)schemeisgreatfullyacknowledged.WeextendourgratitudetoDr.MalcolmJ.Hawkesford,RothamstedResearch,Harpenden,UK,forhisvaluablesuggestionsinpreparingthemanuscript.WealsoacknowledgethesupportfromDr.MaheshG.Thakkar,HeadoftheDepartment,DepartmentofEarthandEnvironmentalScience,KSKVKachchhuniversity,Bhuj,India,forhispositivesupportinallourendeavours.AuthordetailsDepartmentofEarthandEnvironmentalScience,KSKVKachchhUniversity,MundraRoad,Bhuj370001,Gujarat,India.DepartmentofMicrobiology,PSGVPMandalsArts,ScienceandCommerceCollege,Shahada425409,Maharashtra,India.GujaratInstituteofDesertEcology,Bhuj,Gujarat,India.Received:9May2013Accepted:18September2013Published:31October2013AbrilA,Zurdo-PineiroJL,PeixA,RivasR,VelazquezE(2007)SolubilizationofphosphatebyastrainofRhizobiumleguminosarumisolatedfromPhaseolusvulgarisinElChacoAridosoil(Argentina).In:VelazquezE,Rodriguez-BerruecoC(eds)DevelopmentsinPlantandSoilSciences.Springer,TheNetherlands,pp135AhujaA,GhoshSB,DSouzaSF(2007)Isolationofastarchutilizing,phosphatesolubilizingfungusonbufferedmediumanditscharacterization.BioresourTechnol98:3408AltomareC,NorvellWA,BorjkmanT,HarmanGE(1999)SolubilizationofphosphatesandmicronutrientsbytheplantgrowthpromotingandbiocontrolfungusTrichodermaharzianumRifai22.ApplEnvironMicrobiol65:2926ArmargerN(2002)Geneticallymodifiedbacteriainagriculture.BiochimieAseaPEA,KuceyRMN,StewartJWB(1988)InorganicphosphatesolubilizationbytwoPenicilliumspeciesinsolutioncultureandsoil.SoilBiolBiochemAtlasR,BarthaR(1997)Microbialecology.AddisonWesleyLongman,NewYorketal.SpringerPlusPage11of14http://www.springerplus.com/content/2/1/587 AzamF,MemonGH(1996)Soilorganisms.In:BashirE,BantelR(eds)Soilscience.NationalBookFoundation,Islamabad,pp200BajpaiPD,SundaraRaoWVB(1971)PhosphatesolubilizingbacteriaIII.Soilinoculationwithphosphatesolubilizingbacteria.SoilSciPlantNutr17:46BanikS,DeyBK(1983)Phosphatesolubilizingpotentialityofthemicroorganismscapableofutilizingaluminiumphosphateasasolephosphatesource.ZentralblattMicrobiology138:17BarberSA(1995)Soilnutrientbioavailability.Amechanisticapproach,Wiley,NewYorkBar-YosefB,RogersRD,WolframJH,RichmanE(1999)Pseudomonascepaciarockphosphatesolubilizationinkaoliniteandmontmorillonitesuspensions.SoilSciSocAmJ63:1703BashanY,MorenoM,TroyoE(2000)Growthpromotionoftheseawater-irrigatedoilseedhalophyteSalicorniabigeloviiinoculatedwithmangroverhizospherebacteriaandhalotolerantAzospirillumsp.BiolFertilSoils32:265BashanY,KamnevAA,deBashanLE(2013a)Aproposalforisolatingandtestingphosphate-solubilizingbacteriathatenhanceplantgrowth.BiolFertilSoilsBashanY,KamnevAA,deBashanLE(2013b)Tricalciumphosphateisinappropriateasauniversalselectionfactorforisolatingandtestingphosphate-solubilizingbacteriathatenhanceplantgrowth:aproposalforanalternativeprocedure.BiolFertilSoils49:465BlakeL,MercikS,KoerschensM,MoskalS,PoultonPR,GouldingKWT,WeigelA,PowlsonDS(2000)Phosphoruscontentinsoil,uptakebyplantsandbalanceinthreeEuropeanlong-termfieldexperiments.NutrCyclAgroecosystBolanNS,CurrieLD,BaskaranS(1996)Assessmentoftheinfluenceofphosphatefertilizersonthemicrobialactivityofpasturesoils.BiolFertilSoils21:284ButterlyCR,BunemannEK,McNeillAM,BaldockJA,MarschnerP(2009)Carbonpulsesbutnotphosphoruspulsesarerelatedtodecreaseinmicrobialbiomassduringrepeateddryingandrewettingofsoils.SoilBiolBiochemCaballero-MelladoJ,Onofre-LemusJ,DelosSantosEP,Martinez-AguilarL(2007)Thetomatorhizosphere,anenvironmentrichinnitrogen-fixingBurkholderiaspecieswithcapabilitiesofinterestforagricultureandbioremediation.ApplEnvironMicrobiol73:5308CarrilloAE,LiCY,BashanY(2002)IncreasedacidificationintherhizosphereofcactusseedlingsinducedbyAzospirillumbrasilense.NaturwissenschaftenChandiniTM,DennisP(2002)Microbialactivity,nutrientdynamicsandlitterdecompositioninaCanadianRockyMountainpineforestasaffectedbyNandPfertilizers.ForEcolManage159:187ChenCR,CondronLM,DavisMR,SherlockRR(2003)SeasonalchangesinsoilphosphorusandassociatedmicrobialpropertiesunderadjacentgrasslandandforestinNewZealand.ForestEcolManag117:539ChenYP,RekhaPD,ArunAB,ShenFT,LaiWA,YoungCC(2006)Phosphatesolubilizingbacteriafromsubtropicalsoilandtheirtricalciumphosphatesolubilizingabilities.ApplSoilEcol34:33ChuangCC,KuoYL,ChaoCC,ChaoWL(2007)SolubilizationofinorganicphosphatesandplantgrowthpromotionbyAspergillusniger.BiolFertilSoilsChungH,ParkM,MadhaiyanM,SeshadriS,SongJ,ChoH,SaT(2005)IsolationandcharacterizationofphosphatesolubilizingbacteriafromtherhizosphereofcropplantsofKorea.SoilBiolBiochem37:1970CollavinoMM,SansberroPA,MroginskiLA,AguilarOM(2010)Comparisonofinvitrosolubilizationactivityofdiversephosphate-solubilizingbacterianativetoacidsoilandtheirabilitytopromotePhaseolusvulgarisgrowth.BiolFertilSoils46:727CordellD,DrangertJO,WhiteS(2009)Thestoryofphosphorus:globalfoodsecurityandfoodforthought.GlobEnvironChang19:292CriquetS,FerreE,FarnerEM,LePetitJ(2004)Annualdynamicsofphosphataseactivitiesinanevergreenoaklitterinfluenceofbioticandabioticfactors.SoilBiolBiochem36:1111CrowleyDE(2007)Microbialsiderophoresintheplantrhizosphere.In:BartonLL,AbadiaJ(eds)Ironnutritioninplantsandrhizosphericmicroorganisms.Springer,Dordrecht,pp169DeFreitasJR,BanerjeeMR,GermidaJJ(1997)Phosphate-solubilizingrhizobacteriaenhancethegrowthandyieldbutnotphosphorusuptakeofcanola(BrassicanapusL.).BiolFertilSoils24:358DightonJ,BoddyL(1989)Roleoffungiinnitrogen,phosphorusandsulfurcyclingintemperateforestecosystems.In:BoddyL,MarchantR,ReadD(eds)Nitrogen,phosphorusandsulfurutilizationbyfungi.CambridgeUniversityPress,Cambridge,pp269Di-SimineCD,SayerJA,GaddGM(1998)SolubilizationofzincphosphatebyastrainofPseudomonasfluorescensisolatedfromaforestsoil.BiolFertilSoils28:87DuponnoisR,KisaM,PlenchetteC(2006)PhosphatesolubilizingpotentialoftheArthrobotrysoligospora.JPlantNutrSoilSci169:280EivaziF,TabatabaiMA(1977)Phosphatasesinsoils.SoilBiolBiochem9:167FabreB,ArmauE,EtienneG,LegendreF,TirabyG(1988)Asimplescreeningmethodforinsecticidalsubstancesfromactinomycetes.JAntibiot41:212219FankemH,NwagaD,DeubeA,DiengL,MerbachW,EtoaFX(2006)OccurrenceandfunctioningofphosphatesolubilizingmicroorganismsfromoilpalmtreeElaeisguineensis)rhizosphereinCameroon.AfrJBiotechnol5:2450FeniceM,SeblmanL,FedericiF,VassilevN(2000)ApplicationofencapsulatedPenicilliumvariabileP16insolubilizationofrockphosphate.BioresourTechnol73:157FragaR,RodriguezH,GonzalezT(2001)TransferofthegeneencodingtheNapAacidphosphatasefromMorganellamorganiitoaBurkholderiacepaciastrain.ActaBiotechnol21:359GaurAC,OstwalKP(1972)InfluenceofphosphatedissolvingBacillionyieldandphosphateuptakeofwheatcrop.IndianJExpBiol10:393GerretsonFC(1948)Theinfluenceofmicroorganismsonthephosphorusuptakebyplant.PlantSoil1:51GlickBR(1995)Theenhancementofplantgrowthbyfreelivingbacteria.CanJMicrobiol41:109GoldsteinAH(1994)InvolvementofthequinoproteinglucosedehydrohenaseinthesolubilizationofexogenousphosphatesbyGram-negativebacteria.In:Torriani-GoriniA,YagilandE,SilverS(eds)Phosphateinmicroorganisms:Cellularandmolecularbiology.ASMPress,Washington(DC),pp197GoldsteinAH(1995)Recentprogressinunderstandingthemoleculargeneticsandbiochemistryofcalciumphosphatesolubilizationbygramnegativebacteria.BiolAgricHortic12:185GoldsteinAH,LiuST(1987)MolecularcloningandregulationofamineralphosphatesolubilizinggenefromErwiniaherbicola.Biotechnology5:72GriersonPF,ComerfordNB,JokelaEJ(1998)PhosphorusmineralizationkineticsandresponseofmicrobialphosphorustodryingandrewettinginaFloridaSpodosol.SoilBiolBiochem30:1323GunesA,AtaogluN,TuranM,EsitkenA,KetteringsQM(2009)Effectsofphosphate-solubilizingmicroorganismsonstrawberryyieldandnutrientconcentrations.JPlantNutrSoilSci172:385392GuptaRR,SingalR,ShankerA,KuhadRC,SaxenaRK(1994)Amodifiedplateassayforsecreeningphosphatesolubilizingmicroorganisms.JGenApplMicrobiol40:255GyaneshwarP,NareshKG,ParekhLJ,PoolePS(2002)RoleofsoilmicroorganismsinimprovingPnutritionofplants.PlantSoil245:83HamdaliH,BouizgarneB,HafidiM,LebrihiA,VirolleMJ,OuhdouchY(2008a)ScreeningforrockphosphatesolubilizingActinomycetesfromMoroccanphosphatemines.ApplSoilEcol38:12HamdaliH,HafidiM,VirolleMJ,OuhdouchY(2008b)Growthpromotionandprotectionagainstdamping-offofwheatbytworockphosphatesolubilizingactinomycetesinaP-deficientsoilundergreenhouseconditions.ApplSoilEcol40:510HavlinJ,BeatonJ,TisdaleSL,NelsonW(1999)Soilfertilityandfertilizers.Anintroductiontonutrientmanagement.PrenticeHall,UpperSaddleRiver,NJHeZL,WuJ,ODonnellAG,SyersJK(1997)Seasonalresponsesinmicrobialbiomasscarbon,phosphorusandsulphurinsoilsunderpasture.BiolFertilSoils24:421HwangboH,ParkRD,KimYW,RimYS,ParkKH,KimTH,SuchJS,KimKY(2003)2-ketogluconicacidproductionandphosphatesolubilizationbyEnterobacterintermedium.CurrMicrobiol47:87IllmerPA,SchinnerF(1992)Solubilizationofinorganicphosphatesbymicroorganismsisolatedfromforestsoil.SoilBiolBiochem24:389IllmerPA,SchinnerF(1995)Solubilizationofinorganiccalciumphosphatessolubilizationmechanisms.SoilBiolBiochem27:257IllmerPA,BarbatoA,SchinnerF(1995)SolubilizationofhardlysolubleAlPO4withP-solubilizingmicroorganisms.SoilBiolBiochem27:260IsherwoodKF(2000)MineralFertilizerUseandtheEnvironment.InternationalFertilizerIndustryAssociation/UnitedNationsEnvironmentProgramme,ParisJacobsH,BoswellGP,RitzK,DavidsonFA,GaddGM(2002)Solubilizationofcalciumphosphateasaconsequenceofcarbontranslocationby.FEMSMicrobiolEcol40:65JorqueraMA,HernandezMT,RengelZ,MarschnerP,MoraMD(2008)Isolationofculturablephosphorbacteriawithbothphytate-mineralizationandetal.SpringerPlusPage12of14http://www.springerplus.com/content/2/1/587 phosphate-solubilizationactivityfromtherhizosphereofplantsgrowninavolcanicsoil.BiolFertilSoils44:1025JorqueraMA,CrowleyDE,MarschnerP,GreinerR,FernandezMT,RomeroD,Menezes-BlackburnD,DeLaLuzMoraM(2011)Identificationofb-propellerphytase-encodinggenesinculturablePaenibacillusandbacillussp.fromtherhizosphereofpastureplantsonvolcanicsoils.FEMSMicrobiolEcol75:163172JumaNG,TabatabaiMA(1977)Effectsoftrace-elementsonphosphatase-activityinsoils.SoilSciSocAmJ41:343JumaNG,TabatabaiMA(1998)Hydrolysisoforganicphosphatesbycornandsoybeanroots.PlantSoil107:31KhanMR,KhanSM(2002)Effectofroot-diptreatmentwithcertainphosphatesolubilizingmicroorganisms.BioresourTechnol85(2):213KhanAA,JilaniG,AkhtarMS,NaqviSMS,RasheedM(2009a)Phosphorussolubilizingbacteria:occurrence,mechanismsandtheirroleincropproduction.JAgricBiolSci1(1):48KhanMS,ZaidiA,WaniPA(2009b)Roleofphosphatesolubilisingmicroorganismsinsustainableagriculture.In:LictfouseEetal(eds)SustainableAgriculture.springer,p552,DOI:10.1007/978-90-481-2666-8_34KhanMS,ZaidiA,WaniPA,OvesM(2009c)Roleofplantgrowthpromotingrhizobacteriaintheremediationofmetalcontaminatedsoils.Environchemlett7:1KhanMS,ZaidiA,AhemadM,OvesM,WaniPA(2010)Plantgrowthpromotionbyphosphatesolubilizingfungicurrentperspective.ArchAgronSoilSciKimKY,McDonaldGA,JordanD(1997)SolubilizationofhydroxyapatitebyEnterobacteragglomeransandclonedEscherichiacoliinculturemedium.BiolFertilSoils24:347KimKY,JordanD,McDonaldGA(1998)Enterobacteragglomerans,phosphatesolubilizingbacteria,andmicrobialactivityinsoil:effectofcarbonsources.SoilBiolBiochem30:995KrishnarajPU,KhanujaSPS,SadashivamKV(1998)Mineralphosphatesolubilization(MPS)andmpsgenes-componentsineco-friendlyPfertilization.AbstractsofIndoUSWorkshoponApplicationofBiotechnologyforCleanEnvironmentandEnergy,NationalInstituteofAdvancedStudies,Bangalore,p27KuceyRMN(1983)PhosphatesolubilizingbacteriaandfungiinvariouscultivatedandvirginAlbertasoils.CanJSoilSci63:671KumarV,BehlRK,NarulaN(2001)Establishmentofphosphate-solubilizingstrainsAzotobacterchroococcumintherhizosphereandtheireffectonwheatcultivarsundergreenhouseconditions.MicrobiolRes156:87LindsayWL,VlekPLG,ChienSH(1989)Phosphateminerals.In:DixonJB,WeedSB(eds)Mineralsinsoilenvironment,2ndedn.SoilScienceSocietyofAmerica,Madison,WI,USA.pp,pp1089LopezBR,BashanY,BacilioM(2011)Endophyticbacteriaof,anendemicrock-colonizingcactusoftheSouthernSonoranDesert.ArchMicrobiol193:527MalihaR,SaminaK,NajmaA,SadiaA,FarooqL(2004)Organicacidsproductionandphosphatesolubilizationbyphosphatesolubilizingmicroorganismsunderinvitroconditions.PakJBiolSci7:187McGillWB,ColeCV(1981)ComparativeaspectsofcyclingoforganicC,N,SandPthroughsoilorganicmatter.Geoderma26:267NannipieriP,GiagnoniL,LandiL,RenellaG(2011)Roleofphosphataseenzymesinsoil.In:BunemannE,ObersonA,FrossardE(eds)Phosphorusinaction:Biologicalprocessesinsoilphosphoruscycling.Soilbiology,26.Springer,Heidelberg,pp251NautiyalCS(1999)Anefficientmicrobiologicalgrowthmediumforscreeningofphosphatesolubilizingmicroorganisms.FEMSMicrobiolLett170:265NorrishK,RosserH(1983)Mineralphosphate.In:Soils:anAustralianviewpoint.AcademicPress,Melbourne,CSIRO/London,UK,Australia,pp335OliveiraCA,SaNMH,GomesEA,MarrielIE,ScottiMR,GuimaraesCT,SchaffertRE,AlvesVMC(2009)Assessmentofthemycorrhizalcommunityintherhizosphereofmaize(ZeamaysL.)genotypescontrastingforphosphorusefficiencyintheacidsavannasofBrazilusingdenaturinggradientgelelectrophoresis(DGGE).ApplSoilEcol41:249OmarSA(1998)Theroleofrockphosphatesolubilizingfungiandvesiculararbuscularmycorrhiza(VAM)ingrowthofwheatplantsfertilizedwithrockphosphate.WorldJMicrobiolBiotechnol14:211ParkKH,LeeCY,SonHJ(2009)MechanismofinsolublephosphatesolubilizationbyPseudomonasfluorescensRAF15isolatedfromginsengrhizosphereanditsplantgrowth-promotingactivities.LettApplMicrobiol49:222ParkerDR,ReichmannSM,CrowleyDE(2005)Metalchelationintherhizosphere.In:ZobelRW(ed)Rootsandsoilmanagement:interactionsbetweenrootsandthesoil.Agronomymonographno.48.AmericanSocietyofAgronomy,Madison,pp57ParksEJ,OlsonGJ,BrinckmanFE,BaldiF(1990)Characterizationbyhighperformanceliquidchromatography(HPLC)ofthesolubilizationofphosphorusinironorebyafungus.JIndMicrobiolBiotechnol5:183PatilMG,SayyedRZ,ChaudhariAB,ChincholkarSB(2002)PhosphateSolubilizingMicrobes:APotentialBioinoculantforEfficientUseofPhosphateFertilizers.In:ReddySM,ReddySR,GrishamS(eds)BioinoculantsforSustainableAgricultureandForestry.ScientificPublisher,Jodhpur,pp107PeixA,VelazquezE,Martýnez-MolinaE(2007)Molecularmethodsforbiodiversityanalysisofphosphatesolubilizingmicroorganisms(PSM).In:VelazquezE,Rodrguez-BarruecoC(eds)Firstinternationalmeetingonmicrobialphosphatesolubilization.Springer,Berlin,pp97PikovskayaRI(1948)Mobilizationofphosphorusinsoilinconnectionwithvitalactivityofsomemicrobialspecies.Microbiology17:362PuenteME,BashanY,LiCY,LebskyVK(2004a)Microbialpopulationsandactivitiesintherhizoplaneofrock-weatheringdesertplants.I.Rootcolonizationandweatheringofigneousrocks.PlantBiol6:629PuenteME,LiCY,BashanY(2004b)Microbialpopulationsandactivitiesintherhizoplaneofrock-weatheringdesertplants.II.Growthpromotionofcactusseedlings.PlantBiol6:643PuenteME,LiCY,BashanY(2009a)Rock-degradingendophyticbacteriaincacti.EnvironExpBot66:389PuenteME,LiCY,BashanY(2009b)Endophyticbacteriaincactiseedscanimprovethedevelopmentofcactusseedlings.EnvironExpBot66:402QuiquampoixH,MousainD(2005)Enzymatichydrolysisoforganicphosphorus.In:TurnerBL,FrossardandE,BaldwinDS(eds)Organicphosphorusintheenvironment.CABInternational,WallingfordUK,pp89RenellaG,EgamberdiyevaD,LandiL,MenchM,NannipieriP(2006)MicrobialactivityandhydrolaseactivitiesduringdecompositionofrootexudatesreleasedbyanartificialrootsurfaceinCd-contaminatedsoils.SoilBiolBiochem38:702RengelZ,MarschnerP(2005)Nutrientavailabilityandmanagementintherhizosphere:exploitinggenotypicdifferences.NewPhytology168:305ReyesI,BernierL,SimardRR,AntounH(1999)EffectofnitrogensourceonthesolubilizationofdifferentinorganicphosphatesbyanisolateofandtwoUV-inducedmutants.FEMSMicrobiolEcol28:281ReyesI,BaziramakengaR,BernierL,AntounH(2001)SolubilizationofphosphaterocksandmineralsbyawildtypestrainandtwoUVinducedmutantsofPenicilliumregulosum.SoilBiolBiochem33:1741ReyesI,BernierL,AntounH(2002)RockphosphatesolubilizationandcolonizationofmaizerizospherebywildandgeneticallymodifiedstrainsofPenicilliumrugulosum.MicrobEcol44:39RichardsonAE(1994)Soilmicroorganismsandphosphorusavailability.In:PankhurstCE,DoubeandBM,GuptaVVSR(eds)Soilbiota:managementinsustainablefarmingsystems.CSIRO,Victoria,Australia,pp50RichardsonAE(2001)Prospectsforusingsoilmicroorganismstoimprovetheacquisitionofphosphorusbyplants.AustJPlantPhysiol28:897RichardsonAE,SimpsonRJ(2011)Soilmicroorganismsmediatingphosphorusavailability.PlantPhysiol156:989RichardsonAE,HadobasPA,HayesJE,OHaraCP,SimpsonRJ(2001)Utilizationofphosphorusbypastureplantssuppliedwithmyo-inositolhexaphosphateisenhancedbythepresenceofsoilmicroorganisms.PlantSoil229:47RichardsonAE,BareaJM,McNeillAM,Prigent-CombaretC(2009a)Acquisitionofphosphorusandnitrogenintherhizosphereandplantgrowthpromotionbymicroorganisms.PlantSoil321:305RichardsonAE,HockingPJ,SimpsonRJ,GeorgeTS(2009b)Plantmechanismstooptimizeaccesstosoilphosphorus.CropPastureSci60:124RodriguezH,FragaR(1999)Phosphatesolubilizingbacteriaandtheirroleinplantgrowthpromotion.BiotechnolAdv17:319RodriguezH,FragaR,GonzalezT,BashanY(2006)Geneticsofphosphatesolubilizationanditspotentialapplicationsforimprovingplantgrowth-promotingbacteria.PlantSoil287:15RudolphW(1922)InfluenceofSoxidationupongrowthofsoybeansanditseffectonbacterialfloraofsoil.SoilScil4:247SaberK,NahlaLD,ChedlyA(2005)EffectofPonnoduleformationandNfixationinbean.AgronSustainDev25:389SanchezP,LoganT(1992)Mythsandscienceaboutthechemistryandfertilityofsoilsinthetropics.In:LalR,SanchezP(eds)Mythsandscienceofsoilsofthetropics.SoilScienceSocietyofAmerica,Madison,WI,pp35etal.SpringerPlusPage13of14http://www.springerplus.com/content/2/1/587 SchindlerDW,HeckyRE,FindlayDL,StaintonMP,ParkerBR,PatersonMJ,Beaty KG,LyngM,KasianSEM(2008)Eutrophicationoflakescannotbecontrolled byreducingnitrogeninput:resultsofa37-yearwhole-ecosystem experiment.ProcNatlAcadSciUSA105:11254 11258 SimsJT,PierzynskiGM(2005)Chemistryofphosphorusinsoil.In:TabatabaiAM, SparksDL(eds)Chemicalprocessesinsoil,SSSAbookseries8.SSSA, Madison,pp151 192 SingalR,GuptaR,SaxenaRK(1994)Rockphosphatesolubilizationunderalkaline conditionsby Aspergillusjaponicus and A.foetidus .FoliaMicrobiol39:33 36 SongOR,LeeSJ,LeeYS,LeeSC,KimKK,ChoiYL(2008)Solubilizationof insolubleinorganicphosphateby Burkholderiacepacia Da23isolatedfrom cultivatedsoil.BrazJMicrobiol39:151 156 SperberJI(1958a)Theincidenceofapatite-solubilizingorganismsinthe rhizosphereandsoil.AustJAgrRes9:778 781 SperberJI(1958b)Solubilizationofapatitebysoilmicroorganismsproducing organicacids.AustJAgrRes9:782 787 SrideviM,MallaiahKV,YadavNCS(2007)Phosphatesolubilizationby Rhizobium isolatesfromCrotalariaspecies.JPlantSci2:635 639 SubbaRaoNS(1982)Advancesinagriculturalmicrobiology.OxfordandIBH PublicationsCompany,India,pp229 305 SutherlandIW(2001)Biofilmexopolysaccharides:astrongandstickyframework. Microbiology147:3 9 SwabyR,SperberJI(1958)PhosphateDissolvingMicroorganismsinthe RhizosphereofLegume,NutritionOfLegumes;Proc.Univ.Nottingham5 Th EasterSch.Agril.Sci.(CSIROAdelaide).Soils&Fert22,286(1959):289 294 TahaSM,MahmoudSAZ,El-DamatyAA,AbdEl-HafezAM(1969)Activityof phosphatedissolvingbacteriainEgyptiansoil.PlantSoil31:149 TarafdarJC,YadavRS,MeenaSC(2001)Comparativeefficiencyofacid phosphataseoriginatedfromplantandfungalsources.JPlantNutrSoilSci 164:279 282 TilmanD,FargioneJ,WolffB,D AntonioC,DobsonA,HowarthR,SchindlerD, SchlesingerWH,SimberloffD,WackhamerD(2001)Forecastingagriculturally drivenglobalenvironmentalchange.Science292:281 284 TorsvikV,OvreasL(2002)Microbialdiversityandfunctioninsoil:fromgenesto ecosystems.CurrOpinMicrobiol5:240 245 TroloveSN,HedleyMJ,KirkGJD,BolanNS,LoganathanP(2003)Progressin selectedareasofrhizosphereresearchonPacquisition.AustJSoilRes 41:471 499 VassilevN,VassilevaM,AzconR,MedinaA(2001)Preparationofgel-entrapped mycorrhizalinoculuminthepresenceorabsenceof Yarrowialypolytica . BiotechnolLett23:907 909 VassilevN,VassilevaM,NikolaevaI(2006)SimultaneousP-solubilizingand biocontrolactivityofmicroorganisms:potentialsandfuturetrends. ApplMicrobiolBiotechnol71:137 144 VazquezP,HolguinG,PuenteM,Lopez-cortesA,BashanY(2000)Phosphate solubilizingmicroorganismsassociatedwiththerhizosphereofmangrovesin asemi-aridcoastallagoon.BiolFertilSoils30:460 468 VenkateswarluB,RaoAV,RainaP,AhmadN(1984)Evaluationofphosphorus solubilizationbymicroorganismsisolatedfromaridsoil.JIndianSocSoilSci 32:273 277 VyasP,GulatiA(2009)Organicacidproductioninvitroandplantgrowth promotioninmaizeundercontrolledenvironmentbyphosphate-solubilizing fluorescent Pseudomonas .BMCMicrobiol9:174 WakelinSA,WarrenRA,HarveyPR,RyderMH(2004)Phosphatesolubilizationby Penicillium sp.closelyassociatedwithwheatroots.BiolFertilSoils40:36 43 WaniPA,ZaidiA,KhanAA,KhanMS(2005)Effectofphorateonphosphate solubilizationandindoleaceticacid(IAA)releasingpotentialsofrhizospheric microorganisms.AnnalsPlantProtectionSci13:139 144 WhitelawMA(2000)Growthpromotionofplantsinoculatedwithphosphate solubilizingfungi.AdvAgron69:99 151 WhitelawMA,HardenTJ,HelyarKR(1999)Phosphatesolubilizationin solutionculturebythesoilfungus Penicilliumradicum .SoilBiolBiochem 32:655 665 WidadaJ,DamarjayaDI,KabirunS(2007)Theinteractiveeffectsofarbuscular mycorrhizalfungiandrhizobacteriaonthegrowthandnutrientsuptake ofsorghuminacidsoil.In:Rodriguez -BarruecoC(ed)VelazquezE.First InternationalMeetingonMicrobialP hosphateSolubiliz ation,Springer, pp173 177 YiY,HuangW,GeY(2008)Exopolysaccharide:anovelimportantfactorinthe microbialdissolutionoftricalciumphosphate.WorldJMicrobiolBiotechnol 24:1059 1065 ZaidiA,KhanMS,AhemadM,OvesM,WaniPA(2009)RecentAdvancesinPlant GrowthPromotionbyPhosphate-SolubilizingMicrobes.In:KhanMSetal (eds)MicrobialStrategiesforCropImprovement.Springer-Verlag,Berlin Heidelberg,pp23 50 ZhouK,BinkleyD,DoxtaderKG(1992)Anewmethodforestimatinggross phosphorusmineralizationandimmobilizationratesinsoils.PlantSoil 147:243 250 ZhuF,QuL,HongX,SunX(2011)Isol ationandcharacterizationofa phosphate-solubilizinghalophilicbacterium Kushneria sp.YCWA18from DaqiaoSalternonthecoastofYellowSeaofChina.EvidbaseCompl AlternativeMed615032:6 doi:10.1186/2193-1801-2-587 Citethisarticleas: Sharma etal. : Phosphatesolubilizingmicrobes: sustainableapproachformanagingphosphorusdeficiencyin agriculturalsoils. SpringerPlus 2013 2 :587. Submit your manuscript to a journal and bene t from: 7 Convenient online submission 7 Rigorous peer review 7 Immediate publication on acceptance 7 Open access: articles freely available online 7 High visibility within the eld 7 Retaining the copyright to your article Submit your next manuscript at 7 springeropen.com Sharma etal.SpringerPlus 2013, 2 :587 Page14of14 http://www.springerplus.com/content/2/1/587