Bacterial Strains with Nutrient Mobilisation Ability from Ciuc Mountains (Transylvania Region, Romania)

  • Éva LasloEmail author
  • Éva György
  • Beáta Ábrahám
  • Gyöngyvér Mara


This chapter presents the study about some wild leguminous plant’s nodule and rhizosphere bacteria from Ciuc Mountains with beneficial traits related to mineral nutrition and their multiple plant growth-promoting activities as a part of plant-bacteria interaction.

The isolated bacterial strains have nutrient mobilisation abilities and plant growth stimulation effect as phosphate solubilisation, nitrogen fixation and siderophore and indole-3-acetic acid production. During this study, we identified, on the basis of 16S rDNA sequence, 21 bacterial strains originated from different leguminous plants nodules and rhizosphere. These bacterial strains belong to diverse bacterial genus and were identified as Rhizobium leguminosarum (CM2, CM3, CM9, CM11, CM13, CM14, CM15), Rhizobium yanglingense CM1, Bacillus sp. CM4, Mitsuaria chitosanitabida CM5, Variovorax paradoxus CM6 and CM8, Rhizobium rhizogenes CM7, Sinorhizobium meliloti CM10, Rhizobium etli CM12, Pseudomonas abietaniphila CM16, Pseudomonas brassicacearum CM17, Acinetobacter johnsonii CM18, Ensifer (Sinorhizobium) sp. CM19, Serratia proteamaculans CM20 and Serratia sp. CM21. The present study revealed two interesting strains, Mitsuaria chitosanitabida CM5 and Acinetobacter johnsonii CM18 with beneficial characteristics as improving the availability of different nutrients.

The identified and denotated allochthonous bacterial strains with beneficial characteristics confer beneficial effects to plants as a part of the plant functional diversity and microbial composition and are important in sustainable agriculture.


Beneficial strains Nodule bacteria Rhizospheric bacteria Nutrient mobilisation 


  1. Adesemoye AO, Torbert HA, Kloepper JW (2008) Enhanced plant nutrient use efficiency with PGPR and AMF in an integrated nutrient management system. Can J Microbiol 54:876–886. doi: 10.1139/w08-081 CrossRefPubMedGoogle Scholar
  2. Amakata D, Matsuo Y, Shimono K et al (2005) Mitsuaria chitosanitabida gen. nov., sp. nov., an aerobic, chitosanase-producing member of the “Betaproteobacteria”. Int J Syst Evol Microbiol 55:1927–1932. doi: 10.1099/ijs.0.63629-0 CrossRefPubMedGoogle Scholar
  3. Anand R, Chanway C (2013) N2-fixation and growth promotion in cedar colonized by an endophytic strain of Paenibacillus polymyxa. Biol Fertil Soils 49:235–239. doi: 10.1007/s00374-012-0735-9 CrossRefGoogle Scholar
  4. Babalola OO (2010) Beneficial bacteria of agricultural importance. Biotechnol Lett 32:1559–1570. doi: 10.1007/s10529-010-0347-0 CrossRefPubMedGoogle Scholar
  5. Bardgett RD, Bowman WD, Kaufmann R, Schmidt SK (2005) A temporal approach to linking aboveground and belowground ecology. Trends Ecol Evol 20:634–641. doi: 10.1016/j.tree.2005.08.005 CrossRefPubMedGoogle Scholar
  6. Barret M, Morrissey JP, O’Gara F (2011) Functional genomics analysis of plant growth-promoting rhizobacterial traits involved in rhizosphere competence. Biol Fertil Soils 47:729–743. doi: 10.1007/s00374-011-0605-x CrossRefGoogle Scholar
  7. Bashan Y, Kamnev AA, de-Bashan LE (2013) Tricalcium phosphate is inappropriate as a universal selection factor for isolating and testing phosphate-solubilizing bacteria that enhance plant growth: a proposal for an alternative procedure. Biol Fertil Soils 49:465–479. doi: 10.1007/s00374-012-0737-7 CrossRefGoogle Scholar
  8. Benitez M-S, McSpadden Gardener BB (2009) Linking sequence to function in soil bacteria: sequence–directed isolation of novel bacteria contributing to soilborne plant disease suppression. Appl Environ Microbiol 75:915–924. doi: 10.1128/AEM.01296-08 CrossRefPubMedGoogle Scholar
  9. Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350. doi: 10.1007/s11274-011-0979-9 CrossRefPubMedGoogle Scholar
  10. Biswas JC, Ladha JK, Dazzo FB (2000) Rhizobia inoculation improves nutrient uptake and growth of lowland rice. Soil Sci Soc Am J 64:1644–1650CrossRefGoogle Scholar
  11. Bric JM, Bostock RM, Silverstone SE (1991) Rapid in situ assay for indoleacetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microbiol 57:535–538PubMedPubMedCentralGoogle Scholar
  12. Bulgarelli D, Schlaeppi K, Spaepen S et al (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838. doi: 10.1146/annurev-arplant-050312-120106 CrossRefPubMedGoogle Scholar
  13. Castagno LN, Estrella MJ, Sannazzaro AI et al (2011) Phosphate-solubilization mechanism and in vitro plant growth promotion activity mediated by pantoea eucalypti isolated from lotus tenuis rhizosphere in the Salado River basin (Argentina). J Appl Microbiol 110:1151–1165. doi: 10.1111/j.1365-2672.2011.04968.x CrossRefPubMedGoogle Scholar
  14. Chaiharn M, Lumyong S (2011) Screening and optimization of indole-3-acetic acid production and phosphate solubilization from rhizobacteria aimed at improving plant growth. Curr Microbiol 62:173–181. doi: 10.1007/s00284-010-9674-6 CrossRefPubMedGoogle Scholar
  15. de Souza R, Beneduzi A, Ambrosini A et al (2013) The effect of plant growth-promoting rhizobacteria on the growth of rice (Oryza sativa L.) cropped in southern Brazilian fields. Plant Soil 366:585–603. doi: 10.1007/s11104-012-1430-1 CrossRefGoogle Scholar
  16. de Souza E, Bassani V, Sperotto RA, Granada CE (2016) Inoculation of new rhizobial isolates improve nutrient uptake and growth of bean (Phaseolus vulgaris) and arugula (Eruca sativa). J Sci Food Agric 96:3446–3453. doi: 10.1002/jsfa.7527 CrossRefPubMedGoogle Scholar
  17. Demeter L, Csergő AM, Sándor A, Imecs I, TCs V (2011) Natural treasures of the Csík basin (Depresiunea cicului) and Csík mountains (Munţii ciucului). In: Knowles B (ed) Mountain hay meadows – hotspots of biodiversity and traditional culture. Society of Biology, LondonGoogle Scholar
  18. Drogue B, Doré H, Borland S et al (2012) Which specificity in cooperation between phytostimulating rhizobacteria and plants? Res Microbiol 163:500–510. doi: 10.1016/j.resmic.2012.08.006 CrossRefPubMedGoogle Scholar
  19. Drogue B, Combes-Meynet E, Moënne-Loccoz Y et al (2013) Control of the cooperation between plant growth-promoting Rhizobacteria and crops by rhizosphere signals. In: de Bruijn FJ (ed) Molecular microbial ecology of the rhizosphere, vol 1. Wiley, Hoboken, pp 279–293CrossRefGoogle Scholar
  20. Egamberdieva D (2008) Plant growth promoting properties of rhizobacteria isolated from wheat and pea grown in loamy sand soil. Turk J Biol 32:9–15Google Scholar
  21. Franche C, Lindström K, Elmerich C (2009) Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 321:35–59. doi: 10.1007/s11104-008-9833-8 CrossRefGoogle Scholar
  22. Ghirardi S, Dessaint F, Mazurier S et al (2012) Identification of traits shared by rhizosphere-competent strains of fluorescent pseudomonads. Microb Ecol 64:725–737. doi: 10.1007/s00248-012-0065-3 CrossRefPubMedGoogle Scholar
  23. Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012:e963401. doi: 10.6064/2012/963401 CrossRefGoogle Scholar
  24. Granada CE, Arruda L, Lisboa BB et al (2014) Diversity of native rhizobia isolated in south Brazil and their growth promotion effect on white clover (Trifolium repens) and rice (Oryza sativa) plants. Biol Fertil Soils 50:123–132. doi: 10.1007/s00374-013-0840-4 CrossRefGoogle Scholar
  25. Grigulis K, Lavorel S, Krainer U et al (2013) Relative contributions of plant traits and soil microbial properties to mountain grassland ecosystem services. J Ecol 101:47–57. doi: 10.1111/1365-2745.12014 CrossRefGoogle Scholar
  26. Hosseinkhani B, Emtiazi G, Nahvi I (2009) Analysis of phytase producing bacteria (Pseudomonas sp.) from poultry faeces and optimization of this enzyme production. Afr J Biotechnol 8(17):4229–4232Google Scholar
  27. Kang S-M, Joo G-J, Hamayun M et al (2009) Gibberellin production and phosphate solubilization by newly isolated strain of Acinetobacter calcoaceticus and its effect on plant growth. Biotechnol Lett 31:277–281. doi: 10.1007/s10529-008-9867-2 CrossRefPubMedGoogle Scholar
  28. Laslo É, György É, Gy M, Szentes S, Salamon RV, András Cs D, Sz L (2012) The management of N and P nutrition of plants using nitrogen fixing and phosphorus solubilizing bacteria. Environ Eng Manag J 11(2):371–375Google Scholar
  29. Lemanceau P, Expert D, Gaymard F et al (2009) Role of iron in plant–microbe interactions. In: Van Loon LC (ed) Advances in botanical research, vol 51. Elsevier. Academic Press, London, pp 491–549Google Scholar
  30. Liu Y, Zuo S, Zou Y et al (2013) Investigation on diversity and population succession dynamics of endophytic bacteria from seeds of maize (Zea mays L., Nongda108) at different growth stages. Ann Microbiol 63:71–79. doi: 10.1007/s13213-012-0446-3 CrossRefGoogle Scholar
  31. Liu FP, Liu HQ, Zhou HL, Dong ZG, Bai XH, Bai P, Qiao JJ (2014) Isolation and characterization of phosphate-solubilizing bacteria from betel nut (Areca Catechu) and their effects on plant growth and phosphorus mobilization in tropical soils. Biol Fertil Soils 50:927–937. doi: 10.1007/s00374-014-0913-z CrossRefGoogle Scholar
  32. Luna MF, Aprea J, Crespo JM, Boiardi JL (2012) Colonization and yield promotion of tomato by Gluconacetobacter diazotrophicus. Appl Soil Ecol 61:225–229. doi: 10.1016/j.apsoil.2011.09.002 CrossRefGoogle Scholar
  33. Martínez OA, Jorquera MA, Crowley DE, Mora ML (2011) Influence of nitrogen fertilisation on pasture culturable rhizobacteria occurrence and the role of environmental factors on their potential PGPR activities. Biol Fertil Soils 47:875–885. doi: 10.1007/s00374-011-0593-x CrossRefGoogle Scholar
  34. Nascimento SB, Lima AM, Borges BN, de Souza CRB (2015) Endophytic bacteria from Piper tuberculatum Jacq.: isolation, molecular characterization, and in vitro screening for the control of fusarium solani f. sp. piperis, the causal agent of root rot disease in black pepper (Piper nigrum L.) Genet Mol Res 14(3):7567–7577CrossRefPubMedGoogle Scholar
  35. Oldal B, Jevcsák I, Kecskés M (2002) A sziderofortermelő képesség szerepe Pseudomonas-törzsek növénypatogén-antagonista hatásának biológiai vizsgálatában. Biokémia 26:57–63Google Scholar
  36. Parmar N, Dufresne J (2011) Beneficial interactions of plant growth promoting rhizosphere microorganisms. In: Singh A, Parmar N, Kuhad RC (eds) Bioaugmentation biostimulation biocontrol. Springer, Berlin, pp 27–42CrossRefGoogle Scholar
  37. Pásztohy Z (2013) The soils and the biological diversity of the Pogány-havasmicroregion.In:International conference papers: mountain hay meadows – economic, social and environmental value.Gyimesközéplok, Romania23–24 May 2013Google Scholar
  38. Patel K, Goswami D, Dhandhukia D, Thakker J (2015) Techniques to study microbial phytohormones. In: Maheshwari DK (ed) Bacterial metabolites in sustainable agroecosystem. Springer, Switzerland, pp 1–27Google Scholar
  39. Pérez-Montaño F, Alías-Villegas C, Bellogín RA et al (2014) Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiol Res 169:325–336. doi: 10.1016/j.micres.2013.09.011 CrossRefPubMedGoogle Scholar
  40. Prosser JI (2002) Molecular and functional diversity in soil micro-organisms. Plant Soil 244:9–17. doi: 10.1023/A:1020208100281 CrossRefGoogle Scholar
  41. Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol 156:989–996. doi: 10.1104/pp.111.175448 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Rico-Martínez M, Medina FG, Marrero JG, Osegueda-Robles S (2014) Biotransformation of diterpenes. RSC Adv 4:10627–10647. doi: 10.1039/C3RA45146A CrossRefGoogle Scholar
  43. Rong X, Gurel FB, Meulia T, Gardener BBM (2012) Draft genome sequences of the biocontrol bacterium Mitsuaria sp. strain H24L5A. J Bacteriol 194:734–735. doi: 10.1128/JB.06537-11 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Sayyed RZ, Chincholkar SB, Reddy MS, Gangurde NS, Patel PR (2013) Siderophore producing PGPR for crop nutrition and phytopathogen suppression. In: Maheshwari DK (ed) Bacteria in agrobiology: disease management. Springer, Heidelberg, pp 449–471CrossRefGoogle Scholar
  45. Sharma S, Gupta R, Dugar G, Srivastava AK (2012) Impact of application of biofertilizers on soil structure and resident microbial community structure and function. In: Maheshwari DK (ed) Bacteria in agrobiology: plant probiotics. Springer, Heidelberg, pp 65–77CrossRefGoogle Scholar
  46. Shi Y, Lou K, Li C (2009) Promotion of plant growth by phytohormone-producing endophytic microbes of sugar beet. Biol Fertil Soils 45:645–653. doi: 10.1007/s00374-009-0376-9 CrossRefGoogle Scholar
  47. Singh B, Satyanarayana T (2012) Plant growth promotion by phytases and phytase-producing microbes due to amelioration in phosphorus availability. In: Satyanarayana T, Johri BN, Prakash A (eds) Microorganisms in sustainable agriculture and biotechnology. Springer, Dordrecht, pp 3–15CrossRefGoogle Scholar
  48. Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448. doi: 10.1111/j.1574-6976.2007.00072.x CrossRefPubMedGoogle Scholar
  49. Trivedi P, Spann T, Wang N (2011) Isolation and characterization of beneficial bacteria associated with citrus roots in Florida. Microb Ecol 62:324–336. doi: 10.1007/s00248-011-9822-y CrossRefPubMedGoogle Scholar
  50. van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310. doi: 10.1111/j.1461-0248.2007.01139.x CrossRefPubMedGoogle Scholar
  51. van derHeijden MGA, Wagg C (2013) Soil microbial diversity and agro-ecosystem functioning. Plant Soil 363:1–5. doi: 10.1007/s11104-012-1545-4 CrossRefGoogle Scholar
  52. Verma JP, Yadav J, Tiwari KN, Kumar A (2013) Effect of indigenous Mesorhizobium spp. and plant growth promoting rhizobacteria on yields and nutrients uptake of chickpea (Cicer arietinum L.) under sustainable agriculture. Ecol Eng 51:282–286. doi: 10.1016/j.ecoleng.2012.12.022 CrossRefGoogle Scholar
  53. Yolcu H, Turan M, Lithourgidis A et al (2011) Effect of plant growth-promoting rhizobacteria and manure on yield and quality characteristics of Italian ryegrass under semi arid conditions. Aust J Crop Sci 5(13):1730–1736Google Scholar
  54. Young C-C, Shen F-T, Singh S (2012) Strategies for the exploration and development of biofertilizer. In: Maheshwari DK (ed) Bacteria in agrobiology: plant probiotics. Plant probiotics. Springer, Berlin, pp 127–139CrossRefGoogle Scholar
  55. Yuan C-L, Mou C-X, Wu W-L, Guo Y-B (2011) Effect of different fertilization treatments on indole-3-acetic acid producing bacteria in soil. J Soils Sediments 11:322–329. doi: 10.1007/s11368-010-0315-2 CrossRefGoogle Scholar
  56. Zhao S, Zhou N, Zhao Z-Y, Zhang K, Wu G-H, Tian C-Y (2016) Isolation of endophytic plant growth-promoting bacteria associated with the halophyte Salicornia europaea and evaluation of their promoting activity under salt stress. Curr Microbiol 73(4):574–581. doi: 10.1007/s00284-016-1096-7 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  • Éva Laslo
    • 1
    Email author
  • Éva György
    • 2
  • Beáta Ábrahám
    • 1
  • Gyöngyvér Mara
    • 1
  1. 1.Faculty of Economics and Socio-Human Sciences and Engineering, Department of BioengineeringSapientia Hungarian University of TransylvaniaMiercurea CiucRomania
  2. 2.Faculty of Economics and Socio-Human Sciences and Engineering, Department of Food ScienceSapientia Hungarian University of TransylvaniaMiercurea CiucRomania

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