Skip to main content
Log in

Identification of Pantoea Phytate-Hydrolyzing Rhizobacteria Based on Their Phenotypic Features and Multilocus Sequence Analysis (MLSA)

  • EXPERIMENTAL ARTICLES
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

Accurate strain identification within the Pantoea genus is difficult due to homologous recombination, which may affect the species boundaries. An integrated approach is presently the most effective one in determining the species of bacteria. Biochemical identification using the API20E system, phylogenetic analysis of the 16S rRNA gene sequences, and MLSA analysis based on partial sequences of the fusA, pyrG, leuS, gyrB, and rpoB genes showed that the soil phytate-hydrolyzing isolates belonged to the genus Pantoea, specifically to the species Pantoea brenneri. It was also established that phytate-hydrolyzing activity of the strains was accompanied by their ability to fix atmospheric nitrogen.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1.
Fig. 2.

Similar content being viewed by others

REFERENCES

  1. Afanasev, M.V., Mironova, L.V., Basov, E.A., Ostyak, A.S., Kulikalova, E.S., Urbanovich, L.Ya., and Balahonov, S.V., MALDI–TOF mass spectrometry in the accelerated identification of microorganisms of the Vibrio genus, Mol. Biol. Microbiol. Virol., 2014, vol. 29, no. 3, pp. 115‒122.

    Google Scholar 

  2. Brady, C., Cleenwerck, I., Venter, S., Vancanneyt, M., Swings, J., and Coutinho, T., Phylogeny and identification of Pantoea species associated with plants, humans and the natural environment based on multilocus sequence analysis (MLSA), Syst. Appl. Microbiol., 2008, vol. 31, pp. 447‒460.

    Article  CAS  Google Scholar 

  3. Chen, C., Xin, K., Liu, H., Cheng, J., Shen, X., Wang, Y., and Zhang, L., Pantoea alhagi, a novel endophytic bacterium with ability to improve growth and drought tolerance in wheat, Sci. Rep., 2017, vol. 7, art. 41564. https://doi.org/10.1038/srep41564

  4. Deletoile, A., Decre, D., Courant, S., Passet, V., Audo, J., Grimont, P., Arlet, G., and Brisse, S., Phylogeny and identification of Pantoea species and typing of Pantoea agglomerans strains by multilocus gene sequencing, J. Clin. Microbiol., 2009, vol. 47, no. 22, pp. 300−310. https://doi.org/10.1128/JCM.01916-08

    Article  CAS  PubMed  Google Scholar 

  5. Doty, S.L., Oakley, B., Xin, G., Kang, J.W., Singleton, G., Khan, Z., Vajzovic, A., and Staley, J.T., Diazotrophic endophytes of native black cottonwood and willow, Symbiosis, 2009, vol. 47, pp. 23–33.

    Article  CAS  Google Scholar 

  6. Dutkiewicz, J., Mackiewicz, B., Lemieszek, M.K., Golec, M., and Milanowski, J., Pantoea agglomerans: a mysterious bacterium of evil and good. Part IV. Beneficial effects, Ann. Agric. Environ. Med., 2016, vol. 23, no. 2, pp. 206–222.

    Article  CAS  Google Scholar 

  7. Gavini, F., Mergaert, J., Beji, A., Mielcarek, C., Izard, D., Kerster, S.K., and De Ley, J., Transfer of Enterobacter agglomerans (Beijerinck 1888) Ewing and Fife 1972 to Pantoea gen. nov. as Pantoea agglomerans comb. nov. and description of Pantoea dispersa sp. nov., Int. J. Syst. Evol. Microbiol., 1989, vol. 39, no. 3, pp. 337‒345.

    Google Scholar 

  8. Gevers, D., Cohan, F.M., Lawrence, J.G., Spratt, B.G., Coenye, T., Feil, E.J., Stackebrandt, E., Van de Peer, Y., Vandamme, P., Thompson, F.L., and Swings, J., Re-evaluating prokaryotic species, Nat. Rev. Microbiol., 2005, vol. 3, no. 9, pp. 733–739.

    Article  CAS  Google Scholar 

  9. Glass, M.B. and Popovic, T., Preliminary evaluation of the API 20NE and RapID NF Plus systems for rapid identification of Burkholderia pseudomallei and B. mallei, J. Clin. Microbiol., 2005, vol. 43, no. 1, pp. 479–483.

    Article  CAS  Google Scholar 

  10. Gonzalez, A.J., Cleenwerck, I., De Vos, P., and Fernandez-Sanz, A.M., Pseudomonas asturiensis sp. nov., isolated from soybean and weeds, Syst. Appl. Microbiol., 2013, vol. 36, no. 5, pp. 320–324.

    Article  CAS  Google Scholar 

  11. Herrera, C., Koutsoudis, M., Wang, X., and Bodman, S., Pantoea stewartii subsp. stewartii exhibits surface motility, which is a critical aspect of stewart’s wilt disease development on maize, Mol. Plant Microbe Interact., 2008, vol. 21, no. 10, pp. 1359‒1370.

    Article  CAS  Google Scholar 

  12. Holmes, D.E., Nevin, K.P., and Lovley, D.R., Comparison of 16S rRNA, nifD, recA, gyrB, rpoB and fusA genes within the family Geobacteraceae fam. nov., Int. J. Syst. Evol. Microbiol., 2004, vol. 54, no. 5, pp. 1591–1599.

    Article  CAS  Google Scholar 

  13. Janda, J.M. and Abbott, S.L., 16S rRNA gene sequencing for bacterial identification in the diagnostic laboratory: pluses, perils, and pitfalls, J. Clin. Microbiol., 2007, vol. 45, pp. 2761–2764.

    Article  CAS  Google Scholar 

  14. Johnson, K.B., Stockwell, V.O., McLaughlin, R., Sugar, D., Loper, J.E., and Roberts, R.G., Effect of antagonistic bacteria on establishment of honey bee-dispersed Erwinia amylovora in pear blossoms and on fire blight control, Phytopathol., 1993, vol. 83, pp. 995–1002.

  15. Loiret, F.G., Ortega, E., Kleiner, D., Ortega-Rodes, P., Rodes, R., and Dong, Z., A putative new endophytic nitrogen-fixing bacterium Pantoea sp. from sugarcane, J. Appl. Microbiol., 2004, vol. 97, no. 3, pp. 504‒511.

    Article  CAS  Google Scholar 

  16. Maiden, M.C., Multilocus sequence typing of bacteria, A-nnu. Rev. Microbiol., 2006, vol. 60, pp. 561–588.

    Article  CAS  Google Scholar 

  17. Manulis, S., Gafni, Y., Clark, E., Zutra, D., Ophir, Y., and Barash, I., Identification of a plasmid DNA probe for detection of strains of Erwinia herbicola pathogenic on Gypsophila paniculata, Phytopathol., 1991, vol. 81, pp. 54–57.

    Article  Google Scholar 

  18. Merbach, W., Ruppel, S., and Schulze, J., Dinitrogen fixation of microbe-plant associations as affected by nitrate and ammonium supply, Isotopes Environ Health Stud., 1997, vol. 33, no. 1, pp. 67‒73.

    CAS  PubMed  Google Scholar 

  19. Palmer, M., Steenkamp, E.T., Coetzee, M.P., Chan, W.Y., van Zyl, E., De Maayer, P., Coutinho, T.A., Blom, J., Smits, T.H., Duffy, B., and Venter, S.N., Phylogenomic resolution of the bacterial genus Pantoea and its relationship with Erwinia and Tatumella, Antonie Van Leeuwenhoek, 2017, vol. 110, no. 10, pp. 1287‒1309.

    Article  Google Scholar 

  20. Pileggi, M., Pileggi, S.A., Olchanheski, L.R., Silva, P.A., Munoz, A.M., Koskinen, W.C., Barber, B., and Sadowsky, M.J., Isolation of mesotrione-degrading bacteria from aquatic environments in Brazil, Chemosphere, 2012, vol. 86, no. 11, pp. 1127–1132.

    Article  CAS  Google Scholar 

  21. Quispel, A., Hellriegel and Wilfarth’s discovery of (symbiotic) nitrogen fixation hundred years ago, in Nitrogen Fixation: Hundred Years ago, Bothe, H., de Bruijn, F.J., and Newton, W.E., Eds., Stuttgart: Fischer, 1988, pp. 3–12.

    Google Scholar 

  22. Smits, T.H.M., Rezzonico, F., Kamber, T., Blom, J., Goesmann, A., Ishimaru, C.A., Frey, J.E., Stockwell, V.O., and Duffy, B., Metabolic versatility and antibacterial metabolite biosynthesis are distinguishing genomic features of the fire blight antagonist Pantoea vagans C9-1, PLoS One, 2011, vol. 6, no. 7, art. е22247.  https://doi.org/10.1371/journal.pone.0022247

  23. Suleimanova, A.D., Beinhauer, A., Valeeva, L.R., Chastukhina, I.B., Balaban, N.P., Shakirov, E.V., Greiner, R., and Sharipova, M.R., Novel glucose-1-phosphatase with high phytase activity and unusual metal ion activation from soil bacterium Pantoea sp. strain 3.5.1, Appl. Environ. Microbiol., 2015, vol. 81, no. 19, pp. 6790‒6799.

    Article  CAS  Google Scholar 

  24. Stackebrandt, E. and Ebers, J., Taxonomic parameters revisited: tarnished gold standards, Microbiol. Today, 2006, vol. 33, pp. 152–155.

    Google Scholar 

  25. Subba, R., Soil Microorganisms and Plant Growth, Oxford and IBH, India, 1977.

    Google Scholar 

  26. Tambong, J.T., Xu, R., Kaneza, C.A., and Nshogozabahizi, J.C., An in-depth analysis of a multilocus phylogeny identifies leuS as a reliable phylogenetic marker for the genus Pantoea, Evol. Bioinform., 2014, vol. 10, pp. 115–125.

    Article  Google Scholar 

  27. Tambong, J.T., Taxogenomics and systematics of the genus Pantoea, Front. Microbiol., 2019, vol. 10, pp. 24‒63.

    Article  Google Scholar 

  28. Thompson, J.D., Higgins, D.G., and Gibson, T.J., CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice, Nucleic Acids Res., 1994, vol. 22, no. 22, pp. 4673‒4680.

    Article  CAS  Google Scholar 

  29. Walterson, A.M. and Stavrinides, J., Pantoea: insights into a highly versatile and diverse genus within the Enterobacteriaceae, FEMS Microbiol. Rev., 2015, vol. 39, no. 6, pp. 968–984.                                                    

    Article  CAS  Google Scholar 

Download references

Funding

The work was carried out within the framework of the State Program for enhancing the competitiveness of the Kazan (Volga Region) Federal University among the world’s leading research and educational centers and supported by the Russian Science Foundation, project no. 19-76-00020.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. D. Suleimanova.

Ethics declarations

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by E. Makeeva

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Suleimanova, A.D., Itkina, D.L., Pudova, D.S. et al. Identification of Pantoea Phytate-Hydrolyzing Rhizobacteria Based on Their Phenotypic Features and Multilocus Sequence Analysis (MLSA). Microbiology 90, 87–95 (2021). https://doi.org/10.1134/S0026261721010112

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261721010112

Keywords:

Navigation