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A novice Achromobacter sp. EMCC1936 strain acts as a plant-growth-promoting agent

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Abstract

Fifteen bacterial isolates were isolated from a watering canal at Al Hadady-Damrou, Kafr El-Sheikh Governorate, Egypt (31.3°N 30.93°E). The screening process was achieved based on nitrogenase activity. The most potent bacterial isolate (B9) was tested as plant-growth-promoting rhizobacteria (PGPR). Ultrastructural, cultural, biochemical characteristics and 16S rDNA partial sequence were used for the isolate identification and characterization. From the 16S rRNA gene sequencing results, the nearest bacterial species to our isolate was Achromobacter marplatensis B2 (T), EU150134.1, with 97% matching. The sequence was submitted to the NCBI website with the accession number GenBank: KM491552.1. In vitro analysis revealed that the isolate under study is non-pathogenic (virulence factors-free) and capable of producing indole acetic acid (IAA), gibberellin (GA3) and solubilizing rock phosphate. Under greenhouse conditions, tomato inoculation with the obtained Achromobacter sp. EMCC1936 significantly increased vegetative growth, yield parameters and endogenous phytohormones content as compared with common free diazotrophic PGPR, Azotobacter chroococcum EMCCN1458. It was deposited in Microbiological Resource Center for public use with number (EMCC1936). Data revealed the importance of soil inoculation with the obtained isolate and of its role in increasing soil enzymatic activity. These features fulfill the isolate to be used as a PGPR for various crops.

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References

  • Abd El-Aal MM, Abd El-Rahman HM (2014) Impact of PGPR and inorganic fertilization on growth and productivity of sweet Ananas Melon. Int J Agric Sci Res (IJASR) 4:11–26

    Google Scholar 

  • Abd El-Azeem SAM (2007) Some plant growth promoting traits of rhizobacteria isolated from Suez Canal region, Egypt. Afr Crop Sci Conf Proc 8:1517–1525

    Google Scholar 

  • Abd El-Malek Y, Ishac YZ (1986) Evaluation of methods used in counting Azotobacter. J Appl Bacteriol 31:267–269

    Article  Google Scholar 

  • Abyar H, Safahieh A, Zolgharnein H, Zamani I (2012) Isolation and identification of Achromobacter denitrifcans and evaluation of its capacity in cadmium removal. Pol J Environ Stud 12:1523–1527

    Google Scholar 

  • Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current prespective. J King Saud Univ Sci 26:1–20

    Article  Google Scholar 

  • Alhamlan FS, Al-Qahtani AA, Al-Ahdal MN (2015) Recommended advanced techniques for waterborne pathogen detection in developing countries. J Infect Dev Ctries 9:128–135. doi:10.3855/jidc.6101

    PubMed  Google Scholar 

  • Aneja KR (2003) Experiments in microbiology plant pathology and biotechnology, 4th edn. New Age International (P) Ltd. Publishers, New Delhi, p 320

    Google Scholar 

  • Bertrand H, Nalin R, Bally R, Marel JCC (2001) Isolation and identification of the most efficient plant growth promoting bacteria associated with canola. Biol Fert Soil 33:152–156

    Article  Google Scholar 

  • Bhosale GP, Bachate SP, Kale SC (2014) Isolation and characterization of arsenate reducing bacteria from the waste water of an electroplating industry. Int J Curr Microbiol Appl Sci 3:444–452

    CAS  Google Scholar 

  • Birnboim HC, Doly J (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7:1513–1523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burns RG, Dick RP (2002) Enzymes in the environment-activity, ecology, and application. Marcel Dekker, New York

    Book  Google Scholar 

  • Chester B, Cooper LH (1979) Achromobacter Species (CDC Group Vd): morphological and biochemical characterization. J Clin Microbiol 9:425–436

    CAS  PubMed  PubMed Central  Google Scholar 

  • Das S, Dash HR, Mangwani N, Chakraborty J, Kumari S (2014) Understanding molecular identification and polyphasic taxonomic approaches for genetic relatedness and phylogenetic relationships of microorganisms. J Microbiol Methods 103:80–100

    Article  CAS  PubMed  Google Scholar 

  • Diloworth MJ (1970) The acetylene reduction method for measuring biological nitrogen fixation. Rhizobium News Lett 15:155

    Google Scholar 

  • Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149

    Article  CAS  Google Scholar 

  • Drancourt M, Bollet C, Carlioz A, Martelin R, Jean-Pierre G, Raoult D (2000) 16S ribosomal DNA sequence analysis of a large collection of environmental and clinical unidentifiable bacterial isolates. J Clin Microbiol 38:3623–3630

    CAS  PubMed  PubMed Central  Google Scholar 

  • Duggan JM, Goldstein SJ, Chenoweth CE, Kauffman CA, Bradley SF (1996) Achromobacter xylosoxidans bacteremia: report of four cases and review of the literature. Clin Infect Dis 23:569–576

    Article  CAS  PubMed  Google Scholar 

  • Duncan DB (1955) Multiple range and multiple F tests. Biometrics 11:1–42

    Article  Google Scholar 

  • Gomez KA, Gomez AA (1984) Statistical procedures for agricultural research. Wiley, New York

    Google Scholar 

  • Gomez-Cerezo J, Suarez I, Rios JJ, Pena P, de Miguel MJ, de Jose M (2003) Achromobacter xylosoxidans bacteremia: a 10-year analysis of 54 cases. Eur J Clin Microbiol Infect Dis 22:360–363

    Article  CAS  PubMed  Google Scholar 

  • Gomila M, Tvrzová L, Teshim A, Sedlácek I, González-Escalona N, Zdráhal Z, Sedo O, González JF, Bennasar A, Moore ER, Lalucat J, Murialdo SE (2011) Achromobacter marplatensis sp. nov., isolated from a pentachlorophenol-contaminated soil. Int J Syst Evol Microbiol 61:2231–2237

    Article  CAS  PubMed  Google Scholar 

  • Gomila M, Prince-Manzano C, Svensson-Stadler L, Busquets A, Erhard M, Martínez DL, Lalucat J, Moore ERB (2014) Genotypic and phenotypic applications for the differentiation and species-level identification of Achromobacter for clinical diagnoses. PLoS One. doi:10.1371/journal.pone.0114356

    Google Scholar 

  • Harrigan WF, MacCance ME (1976) Laboratory methods in food and dairy microbiology. Academic Press, London

    Google Scholar 

  • Hosseny MH, Ahmed MMM (2009) Effect of nitrogen, organic and PGPR on productivity of lettuce (CV. Romaine) in sandy soil under Assuit conditions. Ass Univ Bull Environ Res 12:79–93

    Google Scholar 

  • Hucker GJ, Conn HJ (1923) Methods of Gram staining. Technical. Bulletin of the New York state, Agriculture Experimental Station, New York, p 93

    Google Scholar 

  • Hugh R (1970) A practical approach to the identification of certain non-fermentative Gram negative rods encountered in clinical specimens. J Conf Public Health Lab 33:81–103

    Google Scholar 

  • Hunter RC, Beveridge TJ (2005) High-resolution visualization of Pseudomonas aeruginosa PAO1 biofilms by freeze-substitution transmission electron microscopy. J Bacteriol 187:7619–7630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Inoue H, Nojima H, Okayama H (1990) High efficiency transformation of Escherichia coli with plasmids. Gene 96:23–28

    Article  CAS  PubMed  Google Scholar 

  • Jakobsen TH, Hansen MA, Jensen PO, Hansen L, Riber L, Cockburn API, Kolpen M, Hansen CR, Ridderberg W, Eickhardt-Sørensen SR et al (2013) Complete genome sequence of the cystic fibrosis pathogen Achromobacter xylosoxidans NH44784-1996 complies with important pathogenic phenotypes. PLoS One 8:e68484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Janda JM, Abbott SL (2007) 16S rRNA gene sequencing for bacterial identification in the diagnostic laboratory: pluses, perils, and pitfalls. J Clin Microbiol 45:2761–2764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang H, Dong H, Zhang G, Yu B, Chapman LR, Fields MW (2006) Microbial diversity in water and sediment of Lake Chaka, an Athalassohaline lake in northwestern China. Appl Environ Microbiol 72:3832–3845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kersters K, De Ley J (1984) Genus III. Agrobacterium Conn 1942. In: Krieg NR, Holt JG (eds) Bergey’s manual of systematic bacteriology, vol 1. Williams & Wilkins, Baltimore, pp 244–254

    Google Scholar 

  • Khan MS, Zaidi A, Ahmad E (2014) Mechanism of phosphate solubilization and physiological functions of phosphate solubilizing microorganisms. Phosphate solubilising microorganisms: principles and application of microphos technology. Springer, Switzerland, pp 31–62

    Google Scholar 

  • Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J (2012) Introducing EzTaxon: a prokaryotic 16S rRNA Gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721

    Article  CAS  PubMed  Google Scholar 

  • Knippschild M, Schmid EN, Uppenkamp M, Konig E, Meusers P, Brittinger G (1996) Infection by Alcaligenes xylosoxidans subsp. xylosoxidans in neutropenic patients. Oncology 53:258–262

    Article  CAS  PubMed  Google Scholar 

  • Koshioka M, Harda J, Noma M, Sassa T, Ogiama K, Taylor JS, Rood SB, Legge RL, Pharis RP (1983) Reversed phase C18 high performance liquid chromatography of acidic and conjugated gibbberellins. J. Chromatgr 256:101–115

    Article  CAS  Google Scholar 

  • Krishnaraj PU, Dahale S (2014) Mineral phosphate solubilization: concepts and prospects in sustainable agriculture. Proc Indian Natl Sci Acad 80(2):389–405

    Article  Google Scholar 

  • Legrand C, Anaissie E (1992) Bacteremia due to Achromobacter xylosoxidans in patients with cancer. Clin Infect Dis 14:479–484

    Article  CAS  PubMed  Google Scholar 

  • Mareque C, Taulé C, Beracochea M, Battistoni F (2015) Isolation, characterization and plant growth promotion effects of putative bacterial endophytes associated with sweet sorghum (Sorghum bicolor (L) Moench). Ann Microbiol 65:1057–1067. doi:10.1007/s13213-014-0951-7

    Article  CAS  Google Scholar 

  • Matuschek E, Brown DFJ, Kahlmeter G (2014) Development of the EUCAST disk diffusion antimicrobial susceptibility testing method and its implementation in routine microbiology laboratories. Clin Microbiol Infect 20:O255–O266

    Article  CAS  PubMed  Google Scholar 

  • Mazumdar A, Deka M (2013) Isolation of free living nitrogen fixing bacteria from crude oil contaminated soil. Int J Bio-Technol Res (IJBTR) 3(4):69–76 (ISSN 2249-6858)

    Google Scholar 

  • Mganga KZ, Razavi BS, Kuzyakov Y (2015) Microbial and enzymes response to nutrient additions in soils of Mt. Kilimanjaro region depending on land use. Eur J Soil Biol 69:33–40

    Article  CAS  Google Scholar 

  • Naik PR, Raman G, Narayanan KB, Sokthivel N (2008) Assessment of genetic and functional diversity of phosphate solubilising fluorescent Pseudomonas isolates from rhizospheric soil. BMC Microbiol 8(230):1–14

    Google Scholar 

  • Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilising microorganisms. FEMS Microbiol Lett 170:265–270

    Article  CAS  PubMed  Google Scholar 

  • Nguyen C, Yan W, Le TF (1992) Genetic variability phosphate solubilizing activity of the ectomycorrhizal fungus Laccaria bicolor (Maire) P.D. Orton Plant Soil 143:193–199

    Article  CAS  Google Scholar 

  • Nicander B, Stahl U, Bjorkman P, Tillberg E (1993) Immuno affinity co-purification of cytokinins and analysis by high-performance liquid chromatography with ultra violet spectrum deterction. Planta 189:312–320

    Article  CAS  PubMed  Google Scholar 

  • Okafor N, MacRae IC (1973) The influence of moisture level, light, aeration and glucose up on acetylene reduction by a black earth soil. Soil Biol Biochem 5:181–186

    Article  CAS  Google Scholar 

  • Pandya ND, Desai PV (2014) Screening and characterization of GA3 producing Pseudomonas monteilii and its impact on plant growth promotion. Int J Curr Microbiol Appl Sci 3:110–115

    CAS  Google Scholar 

  • Petti CA (2007) Detection and identification of microorganisms by gene amplification and sequencing. Med Microbiol 44:1108–1114

    CAS  Google Scholar 

  • Prabhat JHA, Kumar A (2009) Characterization of novel plant growth promoting endophytic bacterium Achromobacter xylosoxidans from wheat plant. Microb Ecol 58:179–188

    Article  Google Scholar 

  • Ramasamy D, Mishra AK, Lagier Jean-Christophe, Padhmanabhan R, Rossi M, Sentausa E, Raoult D, Fournier Pierre-Edouard (2014) A polyphasic strategy incorporating genomic data for the taxonomic description of novel bacterial species. Int J Syst Evol Microbiol 64:384–391

    Article  PubMed  Google Scholar 

  • Sarwart M, Arshad M, Matens DA, Frankenberger WT (1992) Tryptophan-dependent biosynthesis of auxins in soil. Plant Soil 147:207–215

    Article  Google Scholar 

  • Schinner F, Oehlinger R, Kandeler E, Margesin R (1996) Methods in soil biology. Springer Lab Manuals. Part I:213–241

    Google Scholar 

  • Sivasakthi S, Usharani G, Saranraj P (2014) Biocontrol potentiality of plant growth promoting bacteria (PGPR)—Pseudomonas fluorescens and Bacillus subtilis: a review. Afr J Agric Res 9(16):1265–1277

    Google Scholar 

  • Spilker T, VanDamme P, Lipuma JJ (2013) Identification and distribution of Achromobacter species in cystic fibrosis. J Cyst Fibros 12:298–301

    Article  CAS  PubMed  Google Scholar 

  • Srinivasan R, Karaoz U, Volegova M, MacKichan J, Kato-Maeda M, Miller S, Nadarajan R, Brodie EL, Lynch SV (2015) Use of 16S rRNA gene for identification of a broad range of clinically relevant bacterial pathogens. PLoS One. doi:10.1371/journal.pone0117617

    Google Scholar 

  • Vacheron J, Desbrosses G, Marie-Lara B, Touraine B, Moënne-Loccoz Y, Muller D, Legendre L, Wisniewski-Dyé F, Prigent-Combaret C (2013) Plant growth-promoting rhizobacteria and root system functioning. Front Plant Sci 4:356. doi:10.3389/fpls.2013.00356

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Hal S, Stark D, Marriott D, Harkness J (2008) Achromobacter xylosoxidans subsp. xylosoxidans prosthetic aortic valve infective endocarditis and aortic root abscesses. J Med Microbiol 57:525–527

    Article  PubMed  Google Scholar 

  • Vandamme P, Moore ERB, Cnockaert M, De Brandt E, Svensson-Stadler L, Houf K, Spilker T, LiPuma JJ (2013) Achromobacter animicus sp. nov., Achromobacter mucicolens sp. nov., Achromobacter pulmonis sp. nov. and Achromobacter spiritinus sp. nov., from human clinical samples. Syst Appl Microbiol 36:1–10

    Article  CAS  PubMed  Google Scholar 

  • Vincze T, Posfai J, Roberts RJ (2003) NEBcutter: a program to cleave DNA with restriction enzymes. Nucleic Acids Res 31:3688–3691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wayne LG, Brenner DJ, Colwell RR (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464

    Article  Google Scholar 

  • Wedhastri S, Fardhani DM, Kabirun S, Widada J, Widianto D, Evizal R, Prijambada ID (2013) Legume nodulating bacterium, Achromobacter xylosoxidans found in tropical shrub agroecosystem, Sumatra, Indonesia. Indones J Biotechnol 18:161–167

    Article  Google Scholar 

  • Wellinghausen N, Wirths B, Poppert S (2006) Fluorescence in situ hybridization for rapid identification of Achromobacter xylosoxidans and Alcaligenes faecalis recovered from cystic fibrosis patients. J Clin Microbiol 44:3415–3417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wittmann J, Dreiseikelmann B, Rohde C, Rohde M, Sikorski J (2014) Isolation and characterization of numerous novel phages targeting diverse strains of the ubiquitous and opportunistic pathogen Achromobacter xylosoxidans. PLoS One 9(1):e86935. doi:10.1371/journal.pone.0086935

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu S, Yan G, Mei Y, Tao Z, Qing L, Wei C, Guo L, Magemuti QK, Kai L (2014) Achromobacter marplatensis and application thereof. Google Patents. http://www.google.com/patents/CN103642733A?cl=en

  • Yabuuchi E, Kawamura Y, Kosako Y, Ezaki T (1998) Emendation of the genus Achromobacter and Achromobacter xylosoxidans (Yabuuchi and Yano) and proposal of Achromobacter ruhlandii (Packer and Vishniac) comb. nov., Achromobacter piechaudii (Kiredjian et al.) comb. nov., and Achromobacter xylosoxidans subsp. denitrificans (Ruger and Tan) comb. nov. Microbiol Immunol 42:429–438

    Article  CAS  PubMed  Google Scholar 

  • Zaidi A, Khan MS, Ahemad M, Oves M (2009) Plant growth promotion by phosphate solubilizing bacteria. Acta Microbiol Immunol Hung 56:263–284

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank Prof. Dr. M. Hany Tageldin, Horticulture Dept., Faculty of Agriculture, Benha University, for his kind help and assistance.

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Correspondence to Hoda A. S. El-Garhy.

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Communicated by MJ Reigosa.

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Abdel-Rahman, H.M., Salem, A.A., Moustafa, M.M.A. et al. A novice Achromobacter sp. EMCC1936 strain acts as a plant-growth-promoting agent. Acta Physiol Plant 39, 61 (2017). https://doi.org/10.1007/s11738-017-2360-6

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  • DOI: https://doi.org/10.1007/s11738-017-2360-6

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