Skip to main content
SpringerLink
Log in

Ochrobactrum sp. Pv2Z2 exhibits multiple traits of plant growth promotion, biodegradation and N-acyl-homoserine-lactone quorum sensing

  • Original Article
  • Published:
Annals of Microbiology Aims and scope Submit manuscript

Abstract

Rhizosphere bacteria play a vital role in plant growth, pathogen control, biodegradation and rhizosphere signaling. A motile, rod-shaped bacterium, Pv2Z2, isolated from the nodules of the common bean grown in Tanzanian soil was characterized using a polyphasic approach. The traits assessed included the production of indole-3-acetic acid and N-acyl homoserine lactone (AHL) molecules, solubilization of insoluble phosphate and zinc compounds and biodegradation of a number of toxic compounds. The 16S rRNA sequence of Pv2Z2 (EU399793) showed 99 % homology to Ochrobactrum anthropi isolates (Accession no. AJ867292, AJ867291, AJ867290) from soil samples of wheat root. Phylogenetic analysis showed relatedness to nodulating strain Ochrobactrum cytisi rather than to the clinical/pathogenic type strain of O. anthropi. Moreover, it showed unique fingerprints in the randomly amplified polymorphic DNA (RAPD) and two primers-RAPD assays which were different from those of the pathogenic type strain of O. anthropi. The bacterium produced 6.68 μg/mL-1 indoleacetic acid in the presence of tryptophan, released 25.7 μg/mL-1 phosphorus from inorganic tri-calcium phosphate in the Pikoviskaya’s medium and solubilized zinc sulphate and zinc oxide in the LG1 medium. The production of AHLs (e.g. 3O-C7-HSL, 3OH-C7-HSL) was detected with biosensor strains CV026 using reverse phase thin layer chromatography. The bacterium was able to grow in minimal salt medium supplemented with 100 mg/L each of phenol, 2-bromophenol, 2,4-diamino phenol hydrochloride, 3,4-dimethoxy benzyl alcohol and 4-methoxy benzyl alcohol. Phenol degradation was recorded up to a level of 94 % within 12 days. Inoculation of common bean plants resulted in a significant increase in plant height, fresh/dry weight and nitrogen uptake as compared to non-inoculated plants. The data suggest that the plant growth-promoting and biodegradation potential of this bacterium may be exploited on a large scale. The capacity to produce AHL molecules by members of the Ochrobactrum genus has not been previously reported and needs to be explored in detail.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abbas A, Adams C, Scully N, Glennon J, O'Gara F (2007) A role for TonB1 in biofilm formation and quorum sensing in Pseudomonas aeruginosa. FEMS Microbiol Lett 274(2):269–278

    Article  CAS  PubMed  Google Scholar 

  • Adesemoye AO, Torbert HA, Kloepper JW (2009) Plant Growth-Promoting Rhizobacteria allow reduced application rates of chemical fertilizers. Microbiol Ecol 58:921–929

    Article  CAS  Google Scholar 

  • Afzal M, Iqbal S, Rauf S, Khalid ZM (2007) Characteristics of phenol biodegradation in saline solutions by monocultures of Pseudomonas aeruginosa and Pseudomonas pseudomallei. J Hazard Mater 149(1):60–66

    Article  CAS  PubMed  Google Scholar 

  • Agrawal A, Pandey RS, Sharma B (2010) Water pollution with special reference to pesticide contamination in India. J Water Res Protect 2:432–448

    Article  CAS  Google Scholar 

  • Amer MM (2008) Monitoring of Variation among Faba Bean Rhizobium Isolates: 2. Biodegradation of Herbicide, 3(3,4 Dichlorophenyl) -1-methoxy-1-methylurea. Aust J Basic Appl Sci 2(3):540–548

    CAS  Google Scholar 

  • An D, Danhorn T, Fuqua C, Parsek MR (2006) Quorum sensing and motility mediate interactions between Pseudomonas aeruginosa and Agrobacterium tumefaciens in biofilm cocultures. Proc Natl Acad Sci USA 103(10):3828–3833

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Antunes LC, Ferreira RB (2009) Intercellular communication in bacteria. Crit Rev Microbiol 35(2):69–80

    Article  CAS  PubMed  Google Scholar 

  • Anwar S, Liaquat F, Khan QM, Khalid ZM, Iqbal S (2009) Biodegradation of chlorpyrifos and its hydrolysis product 3,5,6-trichloro-2-pyridinol by Bacillus pumilus strain C2A1. J Hazard Mater 168(1):400–405

    Article  CAS  PubMed  Google Scholar 

  • Asad S, Malik KA, Hafeez FY (1991) Competition between inoculated and indigenous Rhizobium/Bradyrhizobium spp. strains for nodulation of grain and fodder legumes in Pakistan. Biol Fertil Soils 12:107–111

    Article  Google Scholar 

  • Beringer JE (1974) R factor transfer in Rhizobium leguminosarum. J Gen Microbiol 84:188–198

    Google Scholar 

  • Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350

    Article  CAS  PubMed  Google Scholar 

  • Cavalcante VA, Döbereiner J (1988) A new acid-tolerant nitrogen fixing bacterium associated with sugarcane. Plant Soil 108:23–31

    Article  Google Scholar 

  • Chakraborty U, Chakraborty BN, Basnet M, Chakraborty AP (2009) Evaluation of Ochrobactrum anthropi TRS-2 and its talc based formulation for enhancement of growth of tea plants and management of brown root rot disease. J Appl Microbiol 107:625–634

    Article  CAS  PubMed  Google Scholar 

  • Chen WM, Chang JS, Wu CH, Chang SC (2004) Characterization of phenol and trichloroethene degradation by the rhizobium Ralstonia taiwanensis. Res Microbiol 155(8):672–680

    Article  CAS  PubMed  Google Scholar 

  • Compant S, Duffy B, Nowak J, Clement C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71(9):4951–4959

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Czajkowski R, Krzyżanowska D, Karczewska J, Atkinson S, Przysowa J, Lojkowska E, Williams P, Jafra S (2011) Inactivation of AHLs by Ochrobactrum sp. A44 depends on the activity of a novel class of AHL acylase. Environ Microbiol Rep 3(1):59–68

    Article  CAS  PubMed  Google Scholar 

  • El-Sayed W, Ibrahim MK, Abu-Shady M, El-Beih F, Ohmura N, Saiki H, Ando A (2003) Isolation and identification of a novel strain of the genus Ochrobactrum with phenol-degrading activity. J Biosci Bioeng 96(3):310–312

    Article  CAS  PubMed  Google Scholar 

  • Faisal M, Hasnain S (2004) Comparative study of Cr(VI) uptake and reduction in industrial effluent by Ochrobactrum intermedium and Brevibacterium sp. Biotechnol Lett 26:1623–1628

    Article  CAS  PubMed  Google Scholar 

  • Feng YS, Lee CM (2009) The potential of the acetonitrile biodegradation by Mesorhizobium sp. F28. J Hazard Mater 164(2–3):646–650

    Article  CAS  PubMed  Google Scholar 

  • Frassinetti S, Setti L, Corti A, Farrinelli P, Montevecchi P, Vallini G (1998) Biodegradation of dibenzothiophene by a nodulating isolate of Rhizobium meliloti. Can J Microbiol 44(3):289–297

    Article  CAS  PubMed  Google Scholar 

  • Garnett TP, Conn VM, Kaiser BN (2009) Root based approaches to improving nitrogen use efficiency in plants. Plant Cell Environ 32:1272–1283

    Article  CAS  PubMed  Google Scholar 

  • Gordon SA, Weber RP (1951) Colorimetric estimation of indole acetic acid. Plant Physiol 26:192–195

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Greenburg AE, Trussell RL, Clesceri LS (1985) Standard menthods for the examination of water and waste water, 16th edn. American Public Health Association, Washington, DC

  • Hafeez FY, Naeem F, Naeem R, Zaidi AH, Malik KA (2005) Symbiotic effectiveness and bacteriocin production by Rhizobium leguminosarum bv. Viciae isolated from agriculture soils in Faisalabad. Environ Exp Bot 54:142–147

    Article  CAS  Google Scholar 

  • Hafeez FY, Yasmin S, Airan D, Rahman M, Zafar Y, Malik KA (2006) Plant growth-promoting bacteria as biofertilizer. Agron Sustain Dev 26:143–150

    Article  CAS  Google Scholar 

  • Imran A, Hafeez FY, Fruhling A, Schumann P, Malik KA, Stackebrandt E (2010) Ochrobactrum ciceri sp. nov., isolated from nodules of Cicer arietinum. Int J Syst Evol Microbiol 60(7):1548–1553

    Article  CAS  PubMed  Google Scholar 

  • Jafra S, Przysowa J, Czajkowski R, Michta A, Garbeva P, van der Wolf JM (2006) Detection and characterization of bacteria from the potato rhizosphere degrading N-acyl-homoserine lactone. Can J Microbiol 52(10):1006–10015

    Article  CAS  PubMed  Google Scholar 

  • Kantar F, Hafeez FY, Shivakumar BG, Sundaram SP, Tejera NA, Aslam A, Bano A, Raja P (2007) Chickpea: Rhizobium management and nitrogen fixation. In: Yadav SS, Redden R, Chen W, and Sharma B (eds) Chickpea breeding and management. Cormwell Press, Trowbridge, pp 179–192

  • Lebuhn M, Achouak W, Schloter M, Berge O, Meier H, Barakat M, Hartmann A, Heulin T (2000) Taxonomic characterization of Ochrobactrum sp. isolates from soil samples and wheat roots, and description of Ochrobactrum tritici sp. nov. and Ochrobactrum grignonense sp. nov. Int J Syst Evol Microbiol 50:2207–2223

    Article  CAS  PubMed  Google Scholar 

  • Lechner U, Baumbach R, Becker D, Kitunen V, Auling G, Salkinoja-Salonen M (1995) Degradation of 4-chloro-2-methylphenol by an activated sludge isolate and its taxonomic description. Biodegradation 6(2):83–92

    Article  CAS  PubMed  Google Scholar 

  • Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556

    Article  CAS  PubMed  Google Scholar 

  • Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning. A laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor

    Google Scholar 

  • McLean RJ, Pierson LS 3rd, Fuqua C (2004) A simple screening protocol for the identification of quorum signal antagonists. J Microbiol Methods 58(3):351–360

    Article  CAS  PubMed  Google Scholar 

  • Mirza BS, Mirza MS, Bano A, Malik KA (2007) Inoculation of chickpea with Rhizobium isolates from roots and nodules and phytohormone producing Enterobacter strains. Aust J Exp Agric 47:1008–1015

    Article  Google Scholar 

  • Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    Article  CAS  Google Scholar 

  • Parke D, Rynne F, Glenn A (1991) Regulation of phenolic catabolism in Rhizobium leguminosarum biovar trifolii. J Bacteriol 173(17):5546–5550

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pikovskaia RI (1948) Metabolism of phosphorous in soil in connection with vital activity of some microbial species. Microbiology 17:362–370

    Google Scholar 

  • Qiu X, Zhonga Q, Lia M, Baia W, Li B (2007) Biodegradation of P-nitrophenol by methyl parathion-degrading Ochrobactrum sp. B2. Int Biodeterior Biodegrad 59:297–301

    Article  CAS  Google Scholar 

  • Radwan SS, Dashti N, El-Nemr I, Khanafer M (2007) Hydrocarbon utilization by nodule bacteria and plant growth-promoting rhizobacteria. Int J Phytoremed 9(6):475–486

    Article  CAS  Google Scholar 

  • Riaz S, Faisal M, Hasnain S (2010) Cicer arietinum growth promotion by Ochrobactrum intermedium and Bacillus cereus in the presence of CrCl3 and K2CrO4. Ann Microbiol 60:729–733

    Article  CAS  Google Scholar 

  • Sakthivel N, Gnanamanickam SS (1986) Toxicity of Pseudomonas fluorescens towards rice sheath rot pathogen Acrocylindrium oryzae. Curr Sci 5:106–107

    Google Scholar 

  • Seo JS, Keum YS, Harada RM, Li QX (2007) Isolation and characterization of bacteria capable of degrading polycyclic aromatic hydrocarbons (PAHs) and organophosphorus pesticides from PAH-contaminated soil in Hilo, Hawaii. J Agric Food Chem 55(14):5383–5389

    Article  CAS  PubMed  Google Scholar 

  • Shah NH, Hafeez FY, Asad S, Hussain A, Malik KA (1995) Isolation and characterization of indigenous Rhizobium leguminosarum bv viciae nodulating Lens culinaris Medik. from four Pakistani soils. In: Malik KA, Nasim A, Khalid AM (eds) Biotechnology for sustainable development. NIBGE, Faisalabad, pp 211–219

    Google Scholar 

  • Smejkal CW, Seymour FA, Burton SK, Lappin-Scott HM (2003) Characterisation of bacterial cultures enriched on the chlorophenoxyalkanoic acid herbicides 4-(2,4-dichlorophenoxy) butyric acid and 4-(4-chloro-2-methylphenoxy) butyric acid. J Ind Microbiol Biotechnol 30(9):561–567

    Article  CAS  PubMed  Google Scholar 

  • Somasegaran P, Hoben HJ (1994) Handbook for Rhizobia Methods in Legume–Rhizobium Technology. Springer, Heidelberg

    Book  Google Scholar 

  • Steinshamn H, Thuen E, Bleken MA, Brenoe UT, Ekerholt G, Yri C (2004) Utilization of nitrogen (N) and phosphorus (P) in an organic dairy farming system in Norway. Agric Ecosyst Environ 104:509–522

    Article  CAS  Google Scholar 

  • Taminiau B, Daykin M, Swift S, Boschiroli ML, Tibor A, Lestrate P, Bolle XD, O'Callaghan D, Williams P, Letesson JJ (2002) Identification of a quorum-sensing signal molecule in the facultative intracellular pathogen Brucella melitensis. Infect Immun 70(6):3004–3011

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tan ZY, Xu XD, Wang ET, Gao JL, Martinez-Romero E, Chen WX (1997) Phylogenetic and genetic relationships of Mesorhizobium tianshanense and related rhizobia. Int J Syst Bacteriol 47(3):874–879

    Article  CAS  PubMed  Google Scholar 

  • Tien TM, Gaskins MH, Hubbell DH (1979) Plant Ggrowth substances produced by Azospirillum brasilense and their effect on the growth of pearl millet (Pennisetum americanum L.). Appl Environ Microbiol 37(5):1016–1024

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677

    Article  CAS  PubMed  Google Scholar 

  • Vincent JM, Humphrey B (1970) Taxonomically significant group antigens in Rhizobium. J Gen Microbiol 63(3):379–382

    Article  CAS  PubMed  Google Scholar 

  • Wei G, Yu J, Zhu Y, Chen W, Wang L (2008) Characterization of phenol degradation by Rhizobium sp. CCNWTB 701 isolated from Astragalus chrysopterus in mining tailing region. J Hazard Mater 151(1):111–117

    Article  CAS  PubMed  Google Scholar 

  • Williams JGK, Kubelik AR, Livak KJ, Rafalski JA (1990) DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Res 18:6531–6535

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yamada T, Takahama Y, Yamada Y (2008) Biodegradation of 2,4,6-tribromophenol by Ochrobactrum sp. strain TB01. Biosci Biotechnol Biochem 72(5):1264–1271

    Article  CAS  PubMed  Google Scholar 

  • Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory manual for physiological studies of rice, 3rd edn. The International Rice Research Institute, Manila

    Google Scholar 

Download references

Acknowledgements

The authors are grateful to Dr. Allan J. Dowine (JIC. Norwich, UK) for providing reference and indicator strains for the AHL assay and to Dr. Erko Stackebrandt (DSMZ, Germany) for providing the DNA of O. anthropi and other type strains of the genus. The research work was partially supported by IDB-BIRCEN Project on “Use of Biofertilizers for Increasing Sustainable Crop Production in Developing Countries: Establishment of a Biofertilizer Resource Center (BIRCEN) at NIBGE” (2000–2005).

Author information

Authors and Affiliations

  1. National Institute for Biotechnology and Genetic Engineering, P.O. Box 577, Jhang Road, Faisalabad, Pakistan

    Asma Imran, Marryam Jumma Abdulla Saadalla, Sami-Ullah Khan, Muhammad Sajjad Mirza, Kauser Abdulla Malik & Fauzia Yusuf Hafeez

  2. Ministry of Agriculture, Natural Resources, Environment and Co-operatives, Zanzibar, Tanzania

    Marryam Jumma Abdulla Saadalla

  3. FC College University, Lahore, Pakistan

    Kauser Abdulla Malik

  4. COMSTAS Institute of Information Technology, Islamabad, Pakistan

    Fauzia Yusuf Hafeez

Authors
  1. Asma Imran
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marryam Jumma Abdulla Saadalla
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sami-Ullah Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Muhammad Sajjad Mirza
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kauser Abdulla Malik
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fauzia Yusuf Hafeez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Asma Imran or Fauzia Yusuf Hafeez.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Imran, A., Saadalla, M.J.A., Khan, SU. et al. Ochrobactrum sp. Pv2Z2 exhibits multiple traits of plant growth promotion, biodegradation and N-acyl-homoserine-lactone quorum sensing. Ann Microbiol 64, 1797–1806 (2014). https://doi.org/10.1007/s13213-014-0824-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13213-014-0824-0

Keywords

Search

Navigation